oseanologi dan limnologi di indonesia

OSEANOLOGI DAN LIMNOLOGI DI INDONESIA (OLDI) Volume 41, Nomor 3, Desember 2015 Diterbitkan oleh

: Pusat Penelitian Oseanografi dengan Pusat Penelitian Limnologi, LIPI

Pemimpin Redaksi Redaksi Pelaksana

: Prof. Dr. Sri Juwana (Marine Culture) 1. Dr. Giyanto, S.Si, M.Sc. (Statistical Biology- Coral Ecology) : 2. Dr. Livia Rossila Tanjung (Molecular & Fishery Microbiology) 3. Dra. Ricky Rositasari (Micropalaeontology) 4. Dra. Nurul Dhewani Mirah Sjafrie, M.Si. (Coastal Management) 1. Ir. Sulastri (Limnology-Phytoplanktonology) : 2. Dr. Luki Subehi (Hydroclimatology) 3. Nina Hermayani Sadi, S.Si, M.Si. (Chemical Limnology) 4. Prof. Dr. Ir. Sam Wouthuyzen (Fishery Oceanography) 5. Prof. Dr. Ir. Dwi Listyo Rahayu (Taxonomy) 6. Dr. Ir. Safar Dody, M.Si. (Marine Culture)

Anggota Redaksi

Mitra Bestari (Penyunting)

:

01. 02. 03. 04. 05. 06. 07. 08. 09.

Fahmi, M. Phil. Tjandra Chrismadha, M. Phil. Dr. Sigit Anggoro Putro Dwiono Dr. Fauzan Ali Prof. Sonny Koeshedrayana, M.Sc. Prof. Dr. Suharsono Dr. Ir. Yusli Wardiatno, M.Sc. Prof. Dr. Ngurah N. Wiadnyana, DEA Ir. Retno Hartati, M.Sc.

Penyunting Pelaksana

:

1. 2. 3. 4. 5.

Drs. Maruatal Sitompul Indyaswan Tegar Suryaningtyas, S.Si. Fajar Sumi Lestari, A.Md. Deny Yogaswara, A.Md. Suci Lastrini

Email Redaksi

: [email protected]

Alamat Redaksi

: Pusat Penelitian Oseanografi, LIPI Jl. Pasir Putih I, Ancol Timur, Jakarta 11048. Telepon: 021-64713850, 021-64712287 021-64712425 Fax: 021-64711948, 021-64712287

NomorAkreditasi

: 712/AU3/P2MI-LIPI/10/2015, berlaku sampai dengan Agustus 2018.

Pusat Penelitian Limnologi, LIPI Jl. Raya Bogor Km 46, Cibinong, PO Box 422, Bogor 16911. Telepon: 021-8757071/5 Fax: 021-8757076

OLDI terbit tiga kali dalam setahun (April, Agustus dan Desember). OLDI terbit dalam bentuk cetakan dan on line di http://www.limnologi.lipi.go.id Oseanologi dan Limnologi di Indonesia (OLDI) dengan ISSN 0125-9830 adalah jurnal ilmiah yang merupakan pengembangan dari Oseanologi di Indonesia (ODI). ODI pertama kali diterbitkan pada tahun 1974. Kemudian berubah nama menjadi OLDI pada tahun 1993 dan terakreditasi sejak tahun 2006. Petunjuk penulisan naskah dapat dilihat di bagian belakang jurnal ini.

ISSN 0125 – 9830

OSEANOLOGI DAN LIMNOLOGI DI INDONESIA Volume 41, Nomor 3, Desember 2015

PUSATPENELITIAN OSEANOGRAFI PUSAT PENELITIAN LIMNOLOGI LEMBAGA ILMU PENGETAHUAN INDONESIA JAKARTA – BOGOR OLDI

Vol. 41

No.3

Jakarta-Bogor

ISSN

Desember 2015

0125 – 9830

Hal 245-373

NomorAkreditasi: 712/AU3/P2MI-LIPI/10/2015, berlaku sampai dengan Agustus 2018

ISSN 0125 – 9830 OSEANOLOGI DAN LIMNOLOGI DI INDONESIA Volume 41, Nomor 3, Desember 2015 DAFTAR ISI Halaman 1.

2.

3.

4.

5.

6.

7.

8.

9.

10.

Akurasi Model Jones, Model Richter dan Model Klasik pada Analisis Hubungan 245-257 Panjang-Berat Ikan Kakap Lutjanus vitta (The Accuracy of Jones, Richter and Classic Models in the Analysis of Length-Weight Relationship of Brownstripe Red Snapper Lutjanus vitta). Wanwan Kurniawan dan Selvia Oktaviyani Komunitas Fitoplankton di Laut Lamalera, Nusa Tenggara Timur (Phytoplankton 259-267 Communities in the Lamalera Sea, East Nusa Tenggara). Nurul Fitriya dan Muhammad Lukman Penambahan Spirulina ke dalam Diet Formulasi Mampu Memacu Pertumbuhan Rotifera 269-278 sampai 25 Persen ( Addition of Spirulina into Formulated Diet Stimulated the Growth of Rotifer up to 25 Percent). Indyaswan Tegar Suryaningtyas dan Sri Juwana Pengadaptasian Ikan Mujair Oreochromis mossambicus dalam Air Laut sebagai Alternatif 279-289 Umpan Hidup dalam Menunjang Perikanan Huhate (Adaptation of Tilapia Fish Oreochromis mossambicus to Sea Water as an Alternative Live Bait to Support Pole and Line Fisheries). Muhammad Djen Marassabessy Analisis Keseimbangan Jasa Ekosistem Lamun di Pulau Bintan, Provinsi Kepulauan Riau 291-304 (Analysis of Seagrass Ecosystem Service Balance in the Bintan Island of Kepulauan Riau Province). Nurul D. M. Sjafrie, Luky Adrianto, Ario Damar, Mennofatria Boer Pengungkapan Kejadian Pemutihan Karang Tahun 2010 di Perairan Indonesia melalui 305-326 Analisis Suhu Permukaan Laut (Coral Bleaching Incidents of 2010 in Indonesian Waters Revealed trough Analysis of Sea Surface Temperature). Sam Wouthuyzen, Muhammad Abrar, dan Jonas Lorwens Komunitas Makrozoobentos di Dua Tipe Mikrohabitat Danau Tondano (Macrozoobenthos 327-338 Communities in Two Types of Microhabitat of Lake Tondano). Jojok Sudarso, Imroatushshoolikhah, dan Nasrul Muit Long Term Monitoring of Water Quality and Phytoplankton Changes in Lake Maninjau, 339-353 West Sumatra, Indonesia (Monitoring Jangka Panjang Kualitas Air dan Perubahan Fitoplankton di Danau Maninjau, Sumatra Barat, Indonesia). Sulastri, Fachmijany Sulawesty, and Sulung Nomosatriyo Habitat dan Sebaran Spasial Siput Lola (Trochus spp.) di Perairan Pulau Rhun, Kepulauan 355-364 Banda, Maluku (Habitat and Spatial Distribution of Top Shell (Trochus spp.) in Rhun Island Waters, Banda Islands, Maluku). Safar Dody dan Nur Mashita Amiludin Potensi Kanal Perifiton Buatan Dalam Menurunkan Kelebihan Nutrien di Perairan 365-373 Permukaan (Potential of Artificial Periphyton Canal in Reducing Nutrient Excess in Surface Waters). Nofdianto

LONG TERM MONITORING OF WATER QUALITY AND PHYTOPLANKTON CHANGES IN LAKE MANINJAU, WEST SUMATRA, INDONESIA MONITORING JANGKA PANJANG KUALITAS AIR DAN PERUBAHAN FITOPLANKTON DI DANAU MANINJAU, SUMATRA BARAT, INDONESIA Sulastri, Fachmijany Sulawesty, and Sulung Nomosatriyo Research Center for Limnology-Indonesian Institute of Sciences (LIPI), Cibinong16911. Email: [email protected]. Received 17 Desember 2014, Reviewed 11 November 2015, Accepted 17 Desember 2015.

ABSTRACT Lake Maninjau is one of the eutrophic lakes in Indonesia as indicated by the occurrence of Microcystis aeruginosa blooms in 2000 and 2011. This lake has been utilized to generate electric power since 1983 and to develop fish culture in cages since 1990. The fish culture has been suspected of increasing the organic matter and stimulating blue-green algae growth. This study evaluates the water quality and phytoplankton composition changes in Lake Maninjau. The Secchi depth has tended to decrease and showed an annual variability ranges from 5.1 to 0.8 m. Monitoring of the DO concentration showed that the anoxic zone continued to increase to the upper column of waters, from 40 m in May 2006 to 15 m in June and December 2011. pH and conductivity in the surface water tended to increase. The value of pH > 9 was found from August 2009 until April 2014. The trophic state index (TSI) tended to increase, it was mesotrophic (41.9 to 50.9) between 2001 and 2007 and eutrophic (56.2 to 64.4) between 2008 and 2014. Phosphorus tended to increase indicating a phosphorus surplus and nitrogen limitation (0.013 to 0.066 mg.L-1). Phosphorous in the epilimnion from 2001 until 2007 ranged from 0.013 to 0.066 mg.L-1, while from 2008 to 2011 it ranged from 0.032 to 0.075 mg.L-1. There were changes in the phytoplankton composition. In 2001 and 2005 it was dominated by Chrysophyta and Chlorophyta respectively. In 2009 and 2014, phytoplankton was dominated by Cyanophyta. There were changes in water quality and the composition of phytoplankton indicating that Lake Maninjau is continuously becoming more degraded. Keywords: water quality, eutrophication, phytoplankton, Lake Maninjau.

ABSTRAK Danau Maninjau merupakan salah satu danau eutrofik di Indonesia. Kondisi eutrofik diindikasikan oleh terjadinya ledakan populasi alga tahun 2000 dan 2011. Danau Maninjau telah dimanfaatkan sebagai pembangkit tenaga listrik sejak tahun 1983 dan kegiatan budi daya ikan sejak tahun 1990. Kegiatan ini diduga meningkatkan bahan organik dan mendorong pertumbuhan alga biru hijau di Danau Maninjau. Penelitian ini mengevaluasi kualitas air dan perubahan komposisi fitoplankton di Danau Maninjau. Kedalaman Secchi cenderung menurun (5,1-0,8 m) dan menunjukkan adanya variasi tahunan. Hasil monitoring konsentrasi DO menunjukkan zona anoksik semakin bertambah dan terus meningkat ke kolom atas perairan (40 m pada bulan Mei 2006 dan 15 m pada bulan Juni dan Desember 2011). pH dan konduktivitas semakin naik selama pengamatan. Nilai pH > 9 dijumpai dari bulan Agustus 2009 sampai April 2014. Indeks status trofik cenderung meningkat, status mesotrofik (41,9-50,9) dijumpai tahun 2001 sampai 2007 and eutrofik (56,2-64.4) dijumpai tahun 2008 sampai 2014. Konsentrasi fosfor terus meningkat yang mengindikasikan Danau Maninjau kelebihan unsur fosfor dan keterbatasan unsur nitrogen. Unsur fosfor nampaknya merupakan faktor utama penyebab eutrofikasi. Sejak tahun 2001 hingga 2014 terjadi perubahan komposisi fitoplankton, yakni tahun 2001 fitoplankton didominasi oleh Chrysophyta, selanjutnya pada tahun 2005 didominasi oleh Chlorophyta, dan tahun 2009 serta 2014 didominasi oleh Cyanophyta. Terdapat perubahan kualitas air dan komposisi fitoplankton yang mengindikasikan terjadinya degradasi kualitas air di Danau Maninjau. Kata kunci: kualitas air, euttrofikasi, fitoplankton, Danau Mannjau.

339

Oseanologi dan Limnologi di Indonesia, Vol. 41, No. 3, Desember 2015: 339-353 INTRODUCTION Water eutrophication has become a worldwide environmental problem in recent years (Yang et al., 2008). A recent survey showed that in the Asia Pacific region, 54% of lakes are eutrophic. The proportions of eutrophication of lakes found in Europe, Africa, North America, and South America are 53%, 28%, 48%, and 41% respectively (ILEC/Lake Biwa Research Institute, 1988-1993). An article analyzing the present state and trend of eutrophication of lakes in China concluded that lakes throughout the country were commonly undergoing the process of eutrophication and most urban lakes were facing hyper-eutrophication (Xiangcan, 2003). In Indonesia, most of major lakes are also facing environmental problems including eutrophication, sedimentation, and decline in surface area. Lake Rawa Pening has been facing eutrophication problem indicated by the coverage of over 40% of the surface of the lake by a macrophyte, the water hyacinth (Suprobowati et al, 2012). Lake Limboto in North Sulawesi has also been facing sedimentation and reduced surface area (Putra et al., 2013). Indonesia has established that 15 lakes are national priorities that should be restored and conserved in this country (State of Minister of Environment, 2011). As a global environmental issue, eutrophication is characterized by high nitrogen and phosphorus concentrations in water bodies, resulting in excessive growth of phytoplankton and other aquatic plants (Liu et al., 2010). Lake eutrophication is affected by a wide range of anthropogenic and natural factors (Müller et al. in Liu et al., 2010). The potential effect of artificial or cultural eutrophication includes the increase of phytoplankton biomass and macrophyte coverage, a shift to bloom-forming alga species that might be toxic, a decrease of water transparency and increased incidence of fish kill and oxygen decline (Dokulil & Teubner, 2011). Lake Maninjau is one of the 15 Indonesian lakes identified as a National Priority Lakes for conservation (State Minister for the Environment, 2011). This lake has been facing a eutrophication problem indicated by the occurrence of Microcystis aeruginosa blooming in 2000 and a high chlorophyll-a concentration (62.97 µg/L) (Syandri, 2000; Sulastri et al., 2001). This lake has been utilized to generate electric power since 1983. Consequently, the lake water rarely flows

through its natural outlet into Batang Antokan river. A hydrological study reported that by closing its natural outlet and flushing the lake water out through the intake, the outflow changed from the surface layer to sub surface layer (6 until 10 m depth) (Fachrudin et al., 2002). Lake Maninjau has also been utilized to culture the fish in floating cages since 1990. The number of cages has increase continuously to the point where it exceeds the carrying capacity limit. The carrying capacity of this lake for cage culture was estimated at around 1,500 units (Hartoto & Ridwansyah, 2001). The development of fish culture in cages is suspected of increasing the organic material level and stimulating Cyanobacteria growth. One of the plans to control phytoplankton bloom was discharging the lake water through its natural outlet in March 2001. The impact of flushing the lake water through its natural outlet was to change the dominant phytoplankton from Cyanophyta to Chrysophyta (Sulastri, 2002). However, the number of culture cages continuously increased to reach 15,051 units in 2008 (State Minister for the Environment, 2011). The increasing number of fish culture cages was followed by a gradual change of water quality in 2006 from previous year. Moreover, the trophic state also changed from mesotrophic in 2005 to eutrophic in 2006 (Triyanto et al., 2006 in Sulastri et al., 2012). Furthermore, the occurrence of a Cyanobacteria bloom of Microcystis aeruginosa was also reported in 2011 and was indicated by a high concentration of chlorophyll-a (168.7µg.l-1) (Tanjung, 2013). This study aims to determine the water quality condition and phytoplankton composition changes in Lake Maninjau. This work will be hopefully useful for lake management by, for example controlling the nutrient input. METHODOLOGY Site Sampling Lake Maninjau is located in West Sumatra, between 100o 08’5384” E to 100o 14’02.39” E and 0o 14’ 52.50” S to 0o 24’ 12.17”S (Figure 1) at 462 m above sea level, with a surface area of 9,737.50 ha, an average depth of 105.5 m and a maximum depth of 168 m (Fachrudin et al., 2002). The volume of water stored in the lake (V), shore line (L) and shore line development (DL) is 10.33 billion m3, 52.7 km and 1.51 km/km2 respectively (Fachrudin et al., 2010).

340

Long Term Monitoring Of Water Quality ... (Sulastri, F. Sulawesty, & S. Nomosatriyo)

Figure 1. Sampling location. Gambar 1. Lokasi sampling. Table 1. Physical description of research stations. Tabel 1. Deskripsi fisik stasiun pengamatan. Station

Physical description

Bayur

Littoral zone, area for fish culture

Koto Gadang

Littoral zone, area for aquaculture, surrounding area is agricultural Near outlet (Batang Antokan), area for aquaculture Littoral zone, area for aquaculture, surrounding area is human settlement Littoral zone, area for aquaculture

Muko-Muko Sigiran Pandan Sungai Batang DM4 DM7

Littoral zone, area for aquaculture, surrounding area is agricultural Pelagic zone, central part of lake (145 m depth), no aquaculture Pelagic zone, deepest part of lake (165 m depth), no aquaculture

Physical and Chemical Parameters Physical and chemical parameter data was collected at the pelagic and littoral zones that are

Parameter observed Secchi depth, TN, TP, Chlorophyll-a, phytoplankton Secchi depth, TN, TP, Chlorophyll-a, phytoplankton Secchi depth, TN, TP, Chlorophyll-a, phytoplankton Secchi depth, TN, TP, Chlorophyll-a, phytoplankton Secchi depth, TN, TP, Chlorophyll-a, phytoplankton Secchi depth, TN, TP, Chlorophyll-a, phytoplankton Secchi depth, TN, TP, Chlorophyll-a, phytoplankton Secchi depth, TN, TP, Chlorophyll-a, phytoplankton, pH, DO, temperature and conductivity important areas used for cage culture and fishing. The physical description and parameters observed at each station are presented in Table 1. The data

341

Oseanologi dan Limnologi di Indonesia, Vol. 41, No. 3, Desember 2015: 339-353 collection was obtained from monitoring data since 2001 to 2014. Water temperature, pH, DO, and conductivity data was collected using a water quality checker (Horiba U-10), while water transparency was examined by the measurement of the Secchi depth. Water temperature, pH, DO, and conductivity were measured in situ at the pelagic zone of the lake (DM7) at depths of 0, 1, 2, 4, 8, 10, 15, 20, 40 m. Water samples for nutrient and chlorophyll-a analysis were collected using a Kamerrer Bottle sampler. Nutrient parameters (TN and TP) were measured in the pelagic and littoral zone. In the pelagic zone, nutrient samples were collected at the depths 0, 1, 2, 4, 8, 10, 15, 20, 40, 60, 80, 100, 120, and 160 m, while in the littoral and DM4, nutrient samples were collected at the euphotic zone (surface water, Secchi depth, and euphotic depth). Nutrients (Total Nitrogen and Total Phosphorus) and Chlorophyll-a were analyzed at the Hydrochemistry Laboratory, Research Centre for Limnology. Samples of nutrients were preserved according to APHA (1999). Total Nitrogen (TN) was measured using the persulphate digestion method (APHA, 1999), then followed by nitrate-N analysis using the Brucine method (APHA, 1975). Total Phosphorus (TP) was determined using the persulphate digestion method and followed by phosphate-P analysis using the Ascorbic Acid method (APHA, 1975). The concentration of nutrients in the epilimnion zone was presented as the average value of the nutrient concentration at the depth of 0 to 15 m, whereas the concentration of nutrients in the hypolimnion zone was presented as the average value of the nutrient concentration at a depth of 20 m to the bottom. Phytoplankton and Chlorophyll-a Analysis. Phytoplankton data were collected in May, September, and October 2001, May 2005, April and June 2009, and April 2014. Phytoplankton sample was collected at the euphotic zone (surface water, Secchi depth, and euphotic depth) by filtering 2 L of water through a plankton net with a 40 µm mesh size. The samples were preserved with 1% lugol solution for taxonomic study in the laboratory. Phytoplankton species was identified according to Prescott (1951), Scott and Prescott (1961), Baker and Fabro (1999), Gell et al. (1999) using an inverted microscope with a magnification of 400 x. Quantitative analysis of phytoplankton used the Lackey Drop Micro Transect method as presented in APHA (1992).

342

A chlorophyll-a sample was collected at the euphotic zone (from the surface water to euphotic depth) by filtering a 500 mL water sample through a GF/F Whatman glass filter paper and preserved by adding a saturated MgCO3 solution. The filter was ground up and extracted in acetone solution (90%). After centrifugation the supernatant was measured with a spectrophotometer (APHA, 1999). Trophic State Index (TSI) The trophic state index (TSI) was calculated to classify the trophic status of the lake using the equation from Carlson and Simpson (1996). The trophic state index (TSI) of Carlson (1977) used algal biomass as the basis for trophic state classification. Three variables: chlorophyll pigments, Secchi depth, and total phosphorus are independently used to estimate algal biomass. The formulas for calculating the TSI values for Secchi disk, TP, and chlorophyll-a are as follows: TSI for Secchi depth : TSI (SD) = 60 -14.41 ln(SD)

TSI for Chl-a: TSI (CHL) = 9.81 ln(CHL) + 30.6 TSI for P: TSI (TP) = 14.42 ln(TP) + 4.15

RESULT AND DISCUSSION The values of Secchi depth of Lake Maninjau ranged from 5.1 to 0.8 m (Figure 2). The Secchi depth tended to decrease but there was also an annual variability during observation. In general, the value of Secchi depth was higher in 2001, 2002, 2005 and the highest Secchi depth was found in May 2005. In December 2005 the Secchi depth decreased, but then increased again in 2006 and in 2007; and the highest Secchi depth was found in May 2007. In 2009 the Secchi depth decreased and continued to decrease until the lowest value of Secchi depth was found in December 2011. A Secchi depth is known to be influenced by absorption characteristics of the water and its dissolved and particulate matter (Wetzel, 1975). Secchi depth is also influenced by time of day, cloud cover, and wind action (Hutchinson, 1957; Wetzel, 1975). It was reported that there are some important factors that influence Secchi depth such as autochthonous production (the amount of plankton, detritus, etc), allochthonous materials or substances from the tributaries that enter the lake and the amount of resuspended materials from the lake bed via wind action or wave activity (Hakanson & Boulon, 2003) There was no data on Secchi depth recorded in 2003 and 2004, but the highest Secchi

Long Term Monitoring Of Water Quality ... (Sulastri, F. Sulawesty, & S. Nomosatriyo) depth in May 2005 coincided with high phytoplankton density in that year (Figure 8). Since March 2001, the outflow of Lake Maninjau has been discharged through the intake and natural outlet (Batang Antokan). It was a part of the program to control algae blooms in Lake Maninjau. Since that year, discharge through the natural outlet has been managed based on the water level of Lake Maninjau that is influenced by the ground water and precipitation (Wibowo & Ridwansyah in Sulastri, 2010). Therefore, the highest Secchi depths in 2001, 2002, and May 2005 might be related to the higher water level at Lake Maninjau when phytoplankton at the surface layer flowed out through the natural outlet. The

lower Secchi depth in December was apparently related to algae bloom indicated by a high concentration of chlorophyll-a (12.52 µg.L-1) (Figure 5). December was reported as a dry season with a high intensity of solar radiation (Wibowo and Ridwansyah in Sulastri, 2010; Fachrudin et al., 2010). The increase in radiation intensity in the dry season would support phytoplankton production and decrease in Secchi depth. It was reported that phytoplankton community variability in Lake Winnipeg is largely related to climate and the control of nutrients with large blooms of Cyanobacteria occurring in warm or dry years (Kling in Binding et al., 2011).

Figure 2. Secchi Depth at Station DM7 of Lake Maninjau. Gambar 2. Kedalaman Secchi di Stasiun DM7 Danau Maninjau. Lake Maninjau is thermally stratified with the epilimnion zone (the warmer and lighter upper layer) found from depths of 0 to 10 m and from 0 to 20 m in December 2005 and November 2006 (Figure 3). In June 2011, December 2011, and April 2014 the thermocline layer was found at depths of 6 and 8 m. According to Wetzel (2001) in a stable water column and hot weather, the thermocline can occur near the surface layer and when the epilimnion zone is exposed to strong wind, the thermocline layer extends to the deeper layer. The temperature above 30o C at the surface layer was supported by hot weather in December 2011, June 2011, and April 2014. The conductivity of Lake Maninjau was higher in June and December 2011, and in April 2014, compared to previous observations (Figure 2). Conductivity represents ionic concentration in the waters. Talling and Talling (1965) in Harris (1986) found strong correlation between

conductivity and the concentration of major ions (HCO3+CO3, Cl-, SO4+). Furthermore, it was reported that water with higher ionic strength tended to have a higher nutrient concentration (Talling & Talling, 1965 in Harris, 1986). Therefore, the increase of conductivity may be related to the increase of nutrient concentration in the lake because of organic matter input from fish culture. The same phenomenon occurred for the pH in which the value tended to increase with the pH above 9 was observed in June and December 2011, September 2013, and April 2014, especially in the surface and upper column of water (Figure 3). The high pH value might be related to the high nutrient concentration and stimulated algae growth as well as increased photosynthesis. In June 2011 a Microcystis aeruginosa bloom occurred, the pH was above 10 and the temperature was above 30oC in the surface water (Figure 3).

343

Oseanologi dan Limnologi di Indonesia, Vol. 41, No. 3, Desember 2015: 339-353

Figure 3.

Temperature, conductivity, pH, and dissolved oxygen (DO) profiles in Station DM7 of Lake Maninjau. Gambar 3. Profil suhu, konduktivitas, pH dan oksigen terlarut (DO) di stasiun DM7 Danau Maninjau. The dissolved oxygen (DO) profile showed that the anoxic zone increased and rose to the upper water column. In December 2005, anoxic water was found at 40 m depth, while in June and December 2011, September 2013, and April 2014 anoxic water was found at depths of 15 and 18 m respectively (Figure 3). The increase of the anoxic zone may be related to the increasing oxygen needed to decompose organic matter that may be higher in Lake Maninjau. In very productive lakes, the decomposition of sedimenting organic matter will produce an anoxic

344

condition in the hypolimnion zone (a cool and dense deep layer) (Wetzel, 2001). A higer DO level (> 9 mg.L-1) was found in the surface layer in August 2009, June and December 2011. It may be due to increasing photosynthesis activity and DO concentration in the surface water. Total phosphorus tended to increase during observation (Figure 4). In contrast, nitrogen was more stable in the epilimnion zone and tended to decrease in the hypolimnion (Figure 4). It indicated that there was a trend toward a phosphorus surplus and nitrogen limitation, as

Long Term Monitoring Of Water Quality ... (Sulastri, F. Sulawesty, & S. Nomosatriyo) presented in Figure 4. The TN:TP ratio tended to decrease after 2005. The total phosphorous concentration in the hypolimnion was higher than total phosphorus in the epilimnion. The higher phosphorus in the hypolimnion might be related to the phosphorus released from the sediment. Sediment reflected the relative fertility of the lake and contained 0.06 to 10 mg.L-1 of soluble

interstitial phosphate (Goldman & Horn, 1983). As the oxygen content of the water near the sediment interface declined, the release of phosphorus increased as the redox potential decreased (Wetzel, 2001). This fact was supported by the DO profile of Lake Maninjau in which the anoxic condition was found from a depth of 15 m to the bottom of lake (Figure 3).

Figure 4.

Total phosphorous (TP) and total nitrogen (TN) concentration (upper) and TN:TP ratio at station DM7 (lower). Source: Henny & Nomosatriyo (2012). Gambar 4. Konsentrasi total fosfor dan total nitrogen (atas) dan rasio TN;TP di stasiun DM7 (bawah). Sumber: Henny & Nomosatriyo (2012). Chlorophyll-a concentrations fluctuated during observation with the highest (> 100 µg.L1) found in October 2011 (Figure 5), The highest chlorophyll-a concentration at that time was related to the blooming of the blue-green algae Microcystis aeruginosa. According to Harris (1986) there are two driving ecological variables that influence the occurrence of summer nuisance blooms of blue-green algae, which are physical and chemical conditions. The physical condition is estimated from the ratio of the thermocline depth to the mean depth of the lake, while the chemical condition is estimated from ratio of TN:TP. If the ratio of thermocline depth to the mean depth of the lake (M) is lower than 1, it indicates a stable

condition of the water column as the mean depth of lake exceeds the depth of the thermocline. On the other hand, if the M value is more than 1, it indicates strong vertical mixing. Buoyancy regulating species, such as Microcystis aeruginosa, were rarely found at an M value of more than 1.5 indicating a strong preference for a stable water column (Harris, 1986). Smith (1983) in Harris (1996) reported that nitrogen-fixing blue-green algae rarely formed bloom at a TN:TP ratio above 25. Based on this ecological characteristic for nuisance blooms of blue-green algae, the environmental condition of Lake Maninjau supported the occurrence of Microcystis aeruginosa in October 2011. The average depth of

345

Oseanologi dan Limnologi di Indonesia, Vol. 41, No. 3, Desember 2015: 339-353 Lake Maninjau was 105.5 m, while the thermocline layer observed in June and December 2011 was found at 6 to 8 m, and in October 2011 the thermocline layer was found at 5 to 8 m (Tanjung, 2011). This data showed that ratio of thermocline depth and mean depth of the lake M was lower than 1, so that indicated a stable

condition of water column suitable for the buoyancy-regulating species Microcystis aeruginosa. Another environmental parameter was temperature that supported the bloom of Mycrocystis (Figure 4) when it was above 30°C in the surface water (Tanjung, 2011) and the TN: TP ratio was less than 20-25.

Figure 5. Average of chlorophyll-a concentration in euphotic zone. Gambar 5. Konsentrasi klorofil-a rata-rata di zona eufotik. The trophic state index (TSI) calculation based on Carlson and Simpson (1996), changed from mesotrophic to eutrophic (Table 2, Figure 6). In general, the trophic state index of TP was higher than the trophic state index of chlorophyll which was the same as the trophic state index of Secchi depth. According to Carlson and Simpson (1996), this condition indicates that there were some limiting factors for algae biomass development, such as nitrogen concentration and zooplankton grazing or pollution, but algae dominates the light attenuation in the lake. It was also reported that a

change in the Chlorophyll-a/TP ratio was associated with systematic changes in phytoplankton cell size and the structure and efficiency of the food chain (Harris, 1986). In October 2011 TSI (Chl) > TSI (SD) indicated large particulate algae such as Microcystis dominated light attenuation in the lake. The phosphorous surplus and nitrogen limitation in Lake Maninjau suggested that phosphorus is apparently a major factor causing the eutrophication.

Table 2. Trophic state based on TSI score, according to Carlson and Simpson (1996). Tabel 2. Skor status trofik menurut Carlson dan Simpson (1996). TSI < 30 30-40 40-50 50-60 60-70 70- >80

346

Chlorophyll-a (µg.L-1) 155

T-P (µg.L-1) 192

Secchi depth (m) >8 8- 4 4-2 2-1 1 – 0.5 0.5 - < 0.25

Trophic status Ultraoligotrophic Oligotrophic Mesotrophic Eutrophic Eutrophic Hypereutrophic


Figure 6. Trophic State Index (TSI) of Lake Maninjau. Gambar 6. Indeks Status Trofik (TSI) Danau Maninjau. Phytoplankton Composition There was a shift in the phytoplankton composition in Lake Maninjau from time to time. The dominant phytoplankton composition changed from Chrysophyta (diatom) in 2001 to Chlorophyta (green algae) in 2005, and then to Cyanophyta (blue-green algae) in 2009 and 2014 (Figure 7). The changes in the phytoplankton composition could be influenced by hydrological factors, temperature, light intensity, pH, nutrient input, and grazing by zooplankton (Reynold, 1993). A hydrological factor was used to control the algae bloom of Microcystis at Lake Maninjau in March 2001 by flushing the lake water through its natural outlet at Batang Antokan. Its impact showed that the dominant phytoplankton changed from blue-green algae (Cyanophyta) to green algae (Chlorophyta) and then diatoms (Chrysophyta) (Sulastri, 2002). The shifting of the phytoplankton composition in this observation is apparently related to the water quality changes such as pH, temperature, conductivity, and nutrient. Blue-green algae adapts well to a high temperature, ion concentration, and pH. (Harris, 1986; Gordon et al., 2000 in Lopez, 2001). An increase in phosphorus and nitrogen limitation can stimulate the bloom of blue-green algae (Smith, 1983 in Harris, 1986). Other factors that are responsible for the predominance of bloom-forming Cyanobacteria (blue-green algae) during the summer period are water temperature above 25°C, low light intensity in water, low N:P ratio and stability of the water column (Mankiewicz et al., 2003). Furthermore, Chellappa et al. (1998) in Camara et al. (2009) suggested that the high

conductivity and the dominance of Cyanobacteria species (blue-green algae) are an indication of eutrophication of the tropical reservoir ecosystems of Marechal Dutra Reservoir (Sertao region) of the Rio Grande do Norte. The shifting of the dominant phytoplankton from Chrysophyta to Chlorophyta, and then to Cyanophyta (blue-green algae) indicated that the water quality of Lake Maninjau was continuously degrading. The increasing of Cyanophyta also known as Cyanobacteria (bluegreen algae) population is a common consequence of eutrophication in a lake. The factors identified as contributing toward the increasingly harmful cyanobacterial blooms were the excess of nutrients, increasing of aquaculture production, and organic pollution (Paerl et al., 2001 in Ramsdell et al., 2005; Heisler et al., 2008 in Ren et al., 2014). The phytoplankton species composition in Lake Maninjau is outlined in Appendix 1 and the density of dominant species is presented in Figure 8. Synedra ulna, a species belongs to diatoms (Chrysophyta), was dominant in 2001 and was always abundant during observation. Synedra ulna is most dominant in severe nutrient pollution (Bellinger & Sigee, 2010) such as in a small eutrophic lake in Java (Sulastri, 2009). The diatoms (Chrysophytes) can divide rapidly when phosphorus is not limited (Casas et al., 1999 in Khuantrirong & Traichaiyaporn, 2008). As reported by Wehar and Sheath (2003), Chlorophyta was the most diverse group of phytoplankton in Lake Maninjau. Staurastrum sp. and Cosmarum sp. also belong to Chlorophyta,

347

Oseanologi dan Limnologi di Indonesia, Vol. 41, No. 3, Desember 2015: 339-353 dominant in 2001 and 2005 respectively. Staurastrum was one of the common desmids occurring in nutrient-poor (most species) and moderately nutrient-rich lakes, while Cosmarium, which is common is a very widespread and common genus, but some species do occur in more alkaline or nutrient rich areas (Bellinger & Sigee, 2010). Cylindrospermopsis raciborskii, Anabaea affinis, Aphanizomeon, and Planktolyngbia sp. were dominant and abundant species belonging to blue-green algae (Cyanophyta) in 2009 and 2014. The density of those species increased in 2009 and 2014 (Figure 8). The increase of some species of Cyanobacteria indicated that Lake Maninjau has shown some eutrophication and deterioration of water quality. The cyanobacterial blooms caused problems of surface water scum, bad odour, and toxins that can threaten aquatic and human life (Wu et al., 2010 in Ren at al, 2014). Blue-green algae such as Microcystis aeruginosa, Cylindrospermopsis raciborskii, Anabaena, and Oscillatoria were reported as toxic algae (Mankiewicz et al., 2003). The abundance of those species depended on a variety of ecological factors, particularly nutrient status, illumination, turbulence, and temperature. Those species typically increased

with the eutrophication of the lake (Pick & Lean, 1987 in Wehr & Sheath, 2003). In Lake Maninjau, Microcystis bloomed in 2002 and 2011 (Syandri, 2002; Tanjung, 2013). However, this species was not found to be dominant in this observation. It was reported that Microcystis established a massive surface blooms (hyperscums) under eutrophic conditions, low turbulence (calm winds), and high irradiance (Zohary & Breen, 1989 in Wehar & Sheath, 2003). The suitable environmental condition for Microcystis bloom might have occurred in 2001 and 2011. On the other hand, the usual program for controlling algae bloom in Lake Maninjau was discharging the lake water through its natural outlet. In that way, Microcystis floating on the surface flows out together with the surface water causing the population of Microcystis to decrease in the lake. Pyrrhophyta or Dinoflagellate species found in Lake Maninjau are typically minor components of the phytoplankton in lakes and ponds, but sometimes form dense blooms, particularly in the presence of high levels of nitrates and phosphates (Wehr & Sheath, 2003). There were few species of Pyrrhophyta in Lake Maninaju, some species were from Peridinium and Glenodineum.

Figure 7. Phytoplankton composition of Lake Maninjau. Gambar 7. Komposisi fitoplankton Danau Maninjau.

348


Figure 8. Density (individual/L) of some dominant phytoplankton in Lake Maninjau. Gambar 8. Kepadatan beberapa fitoplankton (individu/L) dominan di Danau Maninjau.

CONCLUSION

REFERENCES

There was a change of water quality and phytoplankton composition in Lake Maninjau from 2001 to 2014. The DO profile shows that the anoxic zone increased and rose continuously to the upper column, as pH and conductivity tended to increase in the epilimnion. The trophic status changed from mesotrophic to eutrophic. Phosphorus tended to increase indicating a phosphorus surplus and nitrogen limitation. Phosphorus was apparently a major factor causing the eutrophication. The dominant phytoplankton changed. The changes in water quality and the shift in dominant phytoplankton species indicated that the water quality of Lake Maninjau is continuously degrading.

APHA. 1975. Standard methods for the examination of water and wastewater. 14th edition. American Public Health Association. Washington. 1193 pp. APHA, 1992. Standard Methods for the Examination of the Water and Waste Water. 17th Edition. APA-AWWA-WPCF. 1100 pp. APHA. 1999. Standard methods for the examination of water and wastewater. 20th edition. American Public Health Association. Washington. Baker, P. D. and L. D. Fabro. 1999. A Guide to identification of common blue-green algae (Cyanoprokaryotes) in Australia. Cooperative R.C. for Freshwater Ecology, Identification Guide, No.25. 43 pp. Binding, C. E., T. A. Greenberg, and R. P. Bukata. 2011. Time series analysis of algal blooms in Lake of the Woods using the MERIS maximum chlorophyll index. Journal of Plankton Research, 33(12): 1847-1852. Bellinger, E. G. and D. C. Sigee. 2010. Freshwater Algae. Identification and Use as Bioindicator. Wiley-Blackwell, UK. 271 pp.

ACKNOWLEDGMENTS We are thankful to the Research Center for Limnology, Indonesian Institute of Sciences for the support to our research. This research is a part of a project titled Dampak Aktivitas Antropogenik terhadap Produktivitas Danau.

349

Oseanologi dan Limnologi di Indonesia, Vol. 41, No. 3, Desember 2015: 339-353 Carlson, R. E. and J. Simpson. 1996. A coordinator’s guide to volunteer lake monitoring methods. North American Lake Management Society. 96 pp. Camara, F. R. A., A. K. A. Lima, O. Rocha, and N. T. Chellappa. 2009. The role of nutrient dynamics on the phytoplankton biomass (chlorophyll-a) of reservoir-channel continuum in a semi-arid tropical region. Acta Limnol. Bras., (21)4: 431-439. Dokulil, M. T. and K. Teubner. 2011. Eutrophication and Climate Change: Present situation and Future Scenarios in EUTROPHICATION: Causes, Consequence, and Control (A. A. Ansari, S. Singh Gill, G. R. Lanza, W. Rast: Eds), Springer Science Business Media B.V. p. 1-6.. ILEC/Lake Biwa Research Institute [Eds] 19881993 Survey of the State of the World'sLakes. Volumes I-IV. International Lake Environment Committee, Otsu and United Nations Environment Programme, Nairobi. Hakanson, L. and V. V. Boulion. 2003. A Model to Predict How Individual Factors Influence Secchi Depth Variations among and within Lakes. Internat. Rev. Hydrobiol, 88(2): 212232. Hachitnson, G. E. 1957. Treatise on Limnology. Vol 1. Wiley and Sons. Inc., NewYork. 1115 pp. Henny, C. and S. Nomosatriyo. 2012. Nutrient dynamics in sulfidic Lake Maninjau, Indonesia: implication of fish cage aquaculture. International Symposium on Southeast Asian Water Environment, November 8-10, 2012, Hanoi Vietnam, 10: 171-176. Liu, W., Q. Zang, and G. Liu. 2010. Eutrophication Related with Geographic Location, Lake Morphology and Climate Change in China. Hydrobiologia, 644: 289– 299. DOI 10.1007/s10750-010-0151-9. Fachrudin, H. Wibowo, L. Subehi, and I. Ridwansyah. 2002. Karakterisasi Hidrologi Danau Maninjau, Sumatra Barat. Prosiding Seminar Nasional Limnologi, Bogor, 22 April 2002. Puslit Limnologi-LIPI, 65-75. Fachrudin, H. Wibowo, I. Ridwansyah, H. Agita, D. Daruati, and A. Hamid. 2010. Kajian Hidroklimatoplogi sebagai Dasar Peringatan Dini Bencana Kematian Massal Ikan di Danau Maninjau, Sumbar. Laporan Akhir. Program Intensif Peneliti dan Perekayasa. Pusat penelitian Limnologi. 42 hlm.

350

Gell, P. A., J. A. Soneman, M. A. Reid, M. A. Illman, and A. J. Sincock. 1999. An Illustrated Key to Common Diatom Genera from Southern Australia. Cooperative Research Centre for Freshwater Ecology Australia, No. 36. 64 pp. Goldman, C. R. and A. J. Horne. 1983. Limnology. Mc-Graw-Hill. Book Company. New York. 464 pp. Harris, G. H. 1986. The phytoplankton Ecology. Sructure, Function and Fluctuation. Chapman and Hall, New York. 384 pp. Khuantrirong, T. and S. Traichaiyaporn. 2008, Diversity and Seasonal Succession of the Phytoplankton Community in Doi Tao Lake, Chiang Mai Province, Northern Thailand, The Natural History Journal of Chulalongkorn University, 8(2): 143-156. State of Minister of Environment. 2011. Profil 15 Danau Prioritas Nasional. 148 hlm. Lopez-Arcilla, A., D. Moreirea, P. Lopez-Garcia, and C. Gueirero. 2004. Phytoplankton diversity and cyanobacterial dominance in hypertrophic shallow lake which produce alkaline pH. Extremophiles, (8): 109-115. Mankiewicz, J., M. Tarczyn Ska, Z. Walter, and M. Zaleswki. 2003. Natural toxins from Cyanobacteria. Acta Biologica Cracoviensia Series Botanica, 45(2): 9–20. Ren, Y., H. Pei, W. Hu, C. Tian, D. Hao, J. Wei, and Y. Feng. 2014. Spatio-temporal distribution pattern of Cyanobacterial community and its relationship with the environmental factors in Hongze Lake, China. Environt. Monit. Assess., DOI 10.1007/s10661-014-3899-y. Reynold, C. S. 1993. Scale of disturbance and their role in plankton ecology. Hydrobiologia, 249: 157-171. Prescott, G. W. 1951. Algae of the Western Great Lakes Area. Crandbrook Institute of Science. Bulletin. No. 31. 949 pp. Putra, S. S., C. Hassan, Djudi, and H. Suryatmojo. 2013. Reservoir Saboworks Solutions in Limboto Lake Sedimentations, Northern Sulawesi, Indonesia. Procedia Environmental Science, (17): 230-239. Syandri, H. 2002. Dampak Karamba Jaring Apung terhadap Kualitas Air Danau Maninjau. Dipresentasi-kan dalam diskusi Panel Pers Club (PPC), Padang 22 November 2000. 13 hlm. Scott, A. M. and G. W. Prescott. 1961. Indonesian Desmid. Hydrobiologia, Vol. XVII.

Long Term Monitoring Of Water Quality ... (Sulastri, F. Sulawesty, & S. Nomosatriyo) Sulastri. 2002. Spatial and Temporal Distribution of Phytoplankton in Lake Maninjau, West Sumatra. Proceeding of the International Symposium on Land Management and Biodiversity in South East Asia. September 17-20, 2002. Bali, Indonesia. p. 403-408. Sulastri. 2009. Karakteristik komunitas fitoplankton dan faktor lingkungan danaudanau kecil di Jawa. Jurnal Penelitian Perikanan Indonesia, 15(2): v-xvii. Sulastri. 2010. Karakterisasi, Potensi dan Pengembangan Konsep Pengelolaan Sumber Daya Perairan Darat. Laporan Teknis. Puslit Limnologi-LIPI 2010. 154 hlm. Sulastri. 2011. Komposisi dan kelimpahan fitoplankton pasca kematian ikan secara massal di Danau Maninjau, Sumatra Barat. Oseanologi dan Limnologi di Indonesia, 27(3): 495-520. Sulastri, D. I. Hartoto, and I. Yuniarti. 2012. Environmental condition, fish resources and management of Lake Maninjau. Indonesia. Fisheries Research Journal, 18(1): 1-12. Suprobowati, T. S., S. Hadisusanto, P. Gell, and A. Zawadski. 2012. The Diatom Stratigraphy of Rawapening Lake, Implying Eutrophication

History. American Journal of Environmental Sciences, 8(3): 334-344. Tanjung, L. R. 2011. Kajian produktivitas dan pengelolaan sumberdaya perairan darat untuk antisipasi perubahan iklim. Laporan Teknis. Puslit Limnologi-LIPI. 75 hlm. Tanjung, L. R. 2013. Kondisi terkini kualitas air dan tingkat kesuburan Danau Maninjau. Oseanologi dan Limnologi di Indonesia, 39(1): 30-38. Wetzel, R. G., 1975. Limnology. W. B. Sounder Company, Toronto. p. 60-65. Wetzel, R. G. 2001. Limnology. Lake and River Ecosystem. Academic Press, New York, London. 1006 pp. Wehr, J. D. and R. G. Sheath. 2003. Freshwater Algae of North America. Identification and Classification. Academic Press. California . USA. 981 pp. Yang, X., W. U. Xiang, H. A. O. Hu-lin, and H. E. Zhen-li. 2008. Review: Mechanisms and Assessment of Water Eutrophication. Journal of Zhejiang University Science B, 9(3): 197209. Xiangcan, J., 2003. Analysis of Eutrophication State and Trend for Lakes in China. J. Limnol., 62(2): 60-66.

351

Oseanologi dan Limnologi di Indonesia, Vol. 41, No. 3, Desember 2015: 339-353 Appendix 1 Species Composition of Phytoplankton in Lake Maninjau during Observation. Year Species Species a b a 2001

Chrysophyta Asteronela sp Cyclotella sp Cymbella sp Diatoma sp D. elongata Denticula sp Eunotia spp Fragillaria sp

2005

* * * *

2009

* *

* * **

* *

F. construens

*

Frustulia sp.

*

Navicula spp

*

*

*

Nitzchia sp Melosira sp

2014

* *

*

*

Synedra sp S. ulna Surirella sp Gomphonema gracile

**** *

***

***

***

*

Pyrrohophyta Glenodineum sp. Peridinium sp. * Peridinium pusilus Peridinium cinctum Glenodineum Borgei (Leman) Glenodineum quadridens Glenodineum Penadiforme Chlorophyta Actinastrum sp. * Asterococus sp. * Ankistrodismus * sp. A. falcatus Coelastrum sp. *

352

2001

Cyanophyta Anabaena sp Anabaenopsis sp. Anabaena affinis Anabaena bergii Aphanizomenon sp Aphanothese sp. Aphanocapsa sp Chroococcus sp. Chroococcus turgidus Chroococcus varius Chroococcus pallidus Coelosphaerium sp. Gomphosphaeria sp. Gomphosphaeria lacustris Microcystis areoigunosa Oscillatoria spp Cylindrospermopsis raciborskii Planktotrix sp. Planktolyngbia sp. Pseudoanabaena sp. Spirulina sp

*

* * *

**

*

Euglenophyta

***

* **

Euglena spp. Phacus spp. Trachelomonas spp. Chlorophyta Quadrigula sp Pediastrum sp

* *

* * *

Year 2005

*

* **** **

2009b

* *** **** * ****

2014

*

* *

*

*

*

* ** *

*

**

*** *

*** ***

****

*** **

* *

**** *

**** ****

*

*

*

* *

*

*

*

*

*

P. duplex P. duplex var reticulatus P. simplex

*

* *

* * *


C.sphaericum C.combricum Cosmarium identatum C.contractum C.ordinatum C. punctulatum C. regnellii

*** * ** * *

** **

C.spinuliferum

***

*

C. perfissum

*

Cosmarium sp Chrysocapsa sp

** *

Cladophora

*

Closterium sp.

*** *

*

Crucigenia sp.

Cladopora sp. Dictyosphaerium sp.

*

* *** *** * **

*

Euastrum sp. Francela sp. * Gonatozygon aquleatum Kirchneriella Nephrochytium * N.obesum

*

Oocystis pusila

*

*

O. lacustris O. crassa O. gigas Chlorophyta O.elliptica O.Ereonosphaeri a Oocystis sp O. parva

Staurastrum vaasii Staurastrum pseudopachyrhynchum Staurasrum playfairi * Staurastrum ophicura Staurastrum zonatum Staurastrum tohopelagiensisi Staurastrum trissacantum Staurastrum identatum Staurastrum megacanthum

*

C. apiculata C.quadrata C. trunctata

*

*

Staurastrum marginatum Staurastrum xanthium Staurastrum sp. *** Spondylosium sp. * Spirogira sp. Stigeoclonium sp. Tetraedron sp. * Tetraedron minimum *** Tetraedron muticum * Treubaria sp. * Ulothrix sp *

* * *

** *

* * ** *

*

*

* **

Rizoclonium * Scenedesmus arcuatus Scenedesmus bijuga Scenedesmus quadricauda Scenedesmus quadricauda var. maximus Scenedesmus elongata Scenedesmus sp ** Staurastrum arachne Staurastrum disentum

Chlorophyta Ulotrix aecuatis Ulotrix subconstricta Zygnema sp Tolypothrix sp.

*** *** *** * *

*

* * * * *

*** *** ** * * * * ** *

* * * * *

* *

* * * *

Note: ****= dominant; ***= abundant; ** = frequent; *= occasional. a: Sulastri (2002); b: Sulastri (2011)

353