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On the relationship between ecology and phytoplankton composition in a karstic spring (Çepni, Bolu)
Ecological Indicators 7 (2007) 497–503 This article is also available online at: www.elsevier.com/locate/ecolind
Short Communication
On the relationship between ecology and phytoplankton composition in a karstic spring (C ¸ epni, Bolu) Abuzer C¸elekli, Okan Ku¨lko¨ylu¨og˘lu * Department of Biology, Faculty of Arts and Science, Abant I˙zzet Baysal University, Go¨lko¨y, TR-14280 Bolu, Turkey Received 23 March 2005; received in revised form 10 February 2006; accepted 23 February 2006
Abstract The phytoplankton assemblages and their relationship to physico-chemical environmental variables were studied in Akkaya spring, a limnocrene type of karstic spring pool, for 14 months from May 2003 to July 2004. A total of 63 taxa, belonging to Bacillariophyta (62%), Chlorophyta (29%), Cyanophyta (3%), Pyrrophyta (3%), Euglenophyta (2%), and Chrysophyta (2%), were found. According to CCA analysis, three environmental variables (conductivity, calcium, and sulphate) had the greatest influence on species composition. Based on their seasonal occurrence, most of the species found closer to the center of CCA diagram had cosmopolitan characteristics, while members of the genus Spirogyra were found together in the fall season. Similar seasonal patterns were also recorded in three other crustacean taxa including Cladocera (Daphnia sp.), Copepoda (Cyclops sp.), and Ostracoda (Fabaeformiscandona fabaeformis). Overall, the first two axes of CCA explained 97% of the relationship between species composition and environmental variables. This result was also supported by UPGMA analysis, where three main groups were clustered based on their binary data and ecological preferences. Although physico-chemical characteristics of the pool changed in the following months, after building of a concrete wall around the pool in October 2003, the long-term effect of such changes are not known at the moment. # 2006 Published by Elsevier Ltd. Keywords: Phytoplankton; Ecological indicators; Karstic spring; CCA; Phenology; Bolu
1. Introduction Phytoplankton compositions are affected by different environmental factors such as pH, light, and temperature (Buzzi, 2002). Besides their importance as the primary producers in food webs and ensuring * Corresponding author. Tel.: +90 374 254 1226; fax: +90 374 253 4642. E-mail address: [email protected] (O. Ku¨lko¨ylu¨og˘lu). 1470-160X/$ – see front matter # 2006 Published by Elsevier Ltd. doi:10.1016/j.ecolind.2006.02.006
ecological balance, species of phytoplankton can be useful indicators of water quality (Kitner and Poulickova, 2003; Rey et al., 2004). Although their capacity as indicator species is commonly recognized in the literature, there are few studies from Turkey. Limnological studies have gained momentum in Turkey in the last decades (e.g. Aykulu et al., 1983; Go¨nu¨lol and Obalı, 1998; Aysel et al., 2002) but far from completion. Most of these studies are based on taxonomic levels above species, but few include
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ecological data at the species level. Except some of the earlier studies on ostracods (Ku¨lko¨ylu¨og˘lu, 2004), there is no study focusing on phytoplankton assemblages in the karstic springs of Turkey. Akkaya spring is one of them, known for its special condition in which water quality and plankton composition seem to be affected by interactions of several chemical components. The purpose of this study was to investigate ecological determinants of phytoplankton composition and their seasonal occurrence in Akkaya spring.
for the identification of non-diatom phytoplankton species. We used canonical correspondence analysis (CCA) to determine the relationships between phytoplankton composition and physico-chemical environmental variables (ter Braak, 1995). A cluster analysis of unweighted pair group mean averages (UPGMA) was applied to discern different taxonomic assemblages among the species. All statistical analyses were conducted using the Multi-Variate Statistical Package (MVSP) program version 3.1 (Kovach, 1998).
2. Materials and methods 3. Results 0
0
Akkaya (C¸epni) spring (318, 31 E, 408, 40 N), 17 km southwest of the Bolu, Turkey is a karstic limnocrene spring located at about 1266 m above sea level (Fig. 1). Monthly samples of phytoplankton were obtained from May 2003 to July 2004 for about 14 months. Five environmental variables were measured in situ by using YSI-85 model oxygen-temperature meter, and pH and redox potential were determined using Hanna model HI-98150 pH/ORP meter. Atmospheric temperature and rainfall values were obtained from Bolu Meteorological Station. Chlorophyll-a concentrations were determined by spectrophotometry after extraction in 90% methanol (Youngman, 1978). Standard methods were used to determine chemical analysis. The taxonomic keys of Krammer and LangeBertalot (1991a,b, 1999a,b) were used for diatom identification, while Prescott (1982), Huber-Pestalozzi (1983), Pfiester and Popovsky (1990), John et al. (2002), and Wehr and Sheath (2002) were followed
Fig. 1. Study site located in the city Bolu, Turkey.
A total of 63 taxa (Table 1), belonging to six divisions Bacillariophyta (62%), Chlorophyta (29%), Cyanophyta (3%), Pyrrophyta (3%), Euglenophyta (2%), and Chrysophyta (2%) were found between May 2003 and July 2004. Among the taxa, Asterionella formosa, Fragilaria capucina, Caloneis silicula, and Spirogyra longata located close to the center of CCA diagram (Fig. 2) were found almost continuously during this study. Maximum numbers of species were identified in summer season, while minimum numbers were recorded in late autumn season. The first group of UPGMA dendogram (Fig. 3) includes seven taxa (Spirogyra communis, S. dubia, S. majuscula, Spirogyra spa., Spirogyra spx., Cocconeis placentula and Peridinium willei). The five species of Spirogyra were generally observed during late summer and fall months. The second group was composed of eight taxa, five of which (Oscillatoria terebiformis, Trachelomonas sp., Ceratium hirundinella, Fragilaria dilata, and Navicula radiosa) were found in moderately nutrient rich waters during the summer season. The third group includes the remaining 32 species, most of which have cosmopolitan characteristics known for their high levels of tolerance to changes in environmental variables. Additionally, three accompanying zooplankton groups (Cladocera, Copepoda, and Ostracoda) were found from Akkaya spring during this study. A Holarctic ostracod species Fabaeformiscandona fabaeformis was found throughout the study, except in the onset of summer 2001, while the species of Cladocera (Cyclops sp.) and Copepoda were encoun-
A. C ¸ elekli, O. Ku¨lko¨ylu¨og˘lu / Ecological Indicators 7 (2007) 497–503 Table 1 Total of 63 phytoplankton species found during 14 months of sampling. Code numbers are the same used in CCA diagram Code
Species
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52
Achnanthes stolida Achnanthes sp. Amphora ovalis Asterionella formosa Aulacoseria granulata Caloneis silicula Cocconeis placentula Cyclotella planctonica Cymatopleura elliptica Cymbella affinis C. cistula C. helvetica C. silesiaca Fragilaria biceps F. capucina F. construens F. crotonensis F. dilata Gomphonema angustum G. parvulum G. truncatum Navicula clementis N. radiosa N. reinhardtii Nitzschia sigmoidea N. vermicularis Stauroneis sp. Chlamydomonas sp. Geminella sp. Gonatozygon brebissoni G. kinahanii Spirogyra communis S. dubia S. fluvitialis S. longata S. majuscula S. mirabilis Spirogyra spa. Spirogyra spx. S. weberi Ulothrix sp. Oscillatoria tenuis O. terebiformis Trachelomonas sp. Ceratium hirundinella Peridinium willei Dinobryon divergens Cymatopleura solea Epithemia adnata Fragilaria ulna F. ulna var. acus Hantzschia amphyoxys
499
Table 1 (Continued ) Code
Species
53 54 55 56 57 58 59 60 61 62 63
Melosira lineata Navicula trivialis Navicula sp. Pinnularia rupestris Rhopalodia gibba Surirella subsalsa Tabellaria sp. Mougeotia parvula M. scalaris Oocystis sp. Roya sp.
tered all year around in the pool. In total, 97% of the relationship between species and environmental variables was explained by the first two axes of CCA. Conductivity, calcium concentrations and sulphate had the greatest influence on the species assemblages (Fig. 2). Physico-chemical variables changed with season and minimum, maximum and mean values of environmental factor are given in Table 2.
4. Discussion and conclusion Finding total of 63 phytoplankton taxa dominated by Bacillariophyta corresponds to earlier studies done in variety of habitats. Indeed, earlier studies stated that Bacillariophyta was the dominant group in Lake Hafik (Kılınc¸, 1998) and in Lake Aygır and Balıklı (S¸ahin, 2000). Compared earlier research, we also found relatively high percentage of Bacillariophyta among the phytoplankton assemblage. It is known that diatoms are generally a dominant group in calcareous regions (Round, 1981). Therefore, the differences in the species composition are possibly due to the difference in the properties of water where extreme conditions are already present in Akkaya spring. The members of phylum have high tolerance towards chemicals and were also found in different habitats in Turkey (Kılınc¸, 1998; Akbulut, 2003). Most of these diatoms (e.g. Cymbella, as calciphilous taxa) known to tolerate different concentrations of Ca(HCO3)2 were also found in water with a high conductivity (Potapova and Charles, 2003). Indeed, finding some of the species of Cymbella close to the vector of calcium in the CCA diagram (Fig. 2) supports this observation.
500
A. C ¸ elekli, O. Ku¨lko¨ylu¨og˘lu / Ecological Indicators 7 (2007) 497–503
Fig. 2. Diagram of canonical correspondence analysis (CCA) shows 14 months, 47 species, and 12 environmental variables. Abbreviations and species codes (numbers) are shown in following Table 1.
During the study period, some species such as A. formosa, F. capucina, and S. longata were found almost all year around. Species richness was increased during summer months, while it decreased during late fall and winter months. It can be consequence of decreasing in water temperature. However, CCA diagram failed to show this effect (Fig. 2). The most diverse genus was Spirogyra (with nine species), most of its members are usually restricted to hard waters. Spirogyra is generally found in soft, slightly acidic waters rich in organic acids. However, some Spirogyra species as seen in our case can also be found in extreme conditions. For example, S. communis was common in the fall season in Akkaya spring. This suggests that the species prefers nutrient rich, calcareous, and slightly acidic waters (John et al., 2002). A. formosa, which was the most common diatom in fall and especially in spring months, has been reported as dominant species even in eutrophic lakes (Nygaard, 1949). Although this species has a high tolerance to extreme water chemistry, its occurrence may be related to its specific phenological characteristics (Round, 1981). In the present study, A. formosa was dominant in April and May 2004 when
phosphate concentrations of the spring water were maximized. CCA analyses suggested that the majority of phytoplankton species have substantial tolerance to different environmental variables. Indeed, among 47 phytoplankton taxa used in the CCA analyses, 24 of them were close to the center of the CCA diagram. This is probably due to the cosmopolitan characteristics of these species (Fig. 2) that indeed, all are known to tolerate large ranges in water qualities. Thus, it seems, overall, phytoplankton assemblage was highly affected by conductivity and calcium concentration (Fig. 2). The dendrogram of UPGMA showed three distinct groups (Fig. 3). In the first one, seven taxa were included (S. communis, S. dubia, S. majuscula, Spirogyra spa, Spirogyra spx, C. placentula, and P. willei). Five species of Spirogyra were generally observed during late summer and fall sampling months. This corresponds with the findings of earlier reports. For example, John et al. (2002) reported that most members of Spirogyra appear in the autumn season and disappear in the summer season. The second clustered group is composed of eight
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Fig. 3. UPGMA dendrogram shows three major clustering groups. Species codes (numbers) are shown in Table 1.
taxa, most of which were reported from moderately nutrient rich waters in the summer months. The third group includes most of the cosmopolitan species located in the center of the CCA diagram (Fig. 2).
Seasonal differences in species composition may be related to rainfall because the amount of rainfall can alter water chemistry including pH. Indeed, the CCA diagram (Fig. 2) showed that rainfall (referring to water precipitation) reflects a negative relationship
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Table 2 The mean, minimum and maximum values of physico-chemical variables measured in Akkaya spring Minimum Maximum Mean Water temperature (8C) 13.9 Air temperature (8C) 1.4 Rainfall (mm) 1.6 Dissolved oxygen (mg/l) 1.93 Saturation (%) 16.2 Conductivity mS/cm 881 Redox potential (Eh) (mV) 5 pH 6.27 Salinity (ppt) 0.4 Turbidity (NTU) 0.2 Chlorophyll-a (mg/l) 0.23 BOD (mg/l) 0.03 HCO3 (meq/l) 23.6 0.009 NO2–N (mg/l) NO3–N (mg/l) 0.006 PO4–P (mg/l) 0.008 NH4–N (mg/l) 0.011 0.26 SO42 (meq/l) Cl (meq/l) 0.69 Ca2+ (meq/l) 25.65
25.1 24.5 97.9 15.5 154.3 2046 41.2 7.76 1 15 7.5 4.05 28 0.046 0.096 0.019 0.115 1.05 10.1 40.01
19.5 12.1 50.9 6.4 69.9 1788 25.6 6.7 0.9 2.1 2.28 1.94 25.7 0.02 0.043 0.01 0.043 0.6 2.88 30.41
n 29 29 29 29 29 29 26 29 29 21 9 12 9 9 6 9 9 9 9 6
with pH and conductivity, but there was a positive relationship between the precipitation and some other variables such as sulphate, nitrite, and phosphate as well. Increasing precipitation seems to cause a decrease in pH level that eventually increases calcium dissolution in the water, which may cause a change in species composition. For example, Cymbella and Achnanthes, which can tolerate such extreme conditions, are known as calciphiles or calcium loving organisms. Consequently, precipitation may have also an important effect on species composition in Akkaya spring. Additionally, anthropogenic factors also play an important role on the habitat structure and species composition in Akkaya spring. Because of its relatively warm water, the area is open for human use such as swimming, bathing, and picnicking. Because of increasing demand by the cities populace, a concrete wall was built around the spring to collect water in a pool. After building this artificial structure, water composition of the spring changed. This action caused some of the species (i.e. F. fabaeformis, a bottom dependent ostracod inhabiting shallow habitats) to disappear from the area. Similar changes were observed in the phytoplankton community in short term, but the long-term effects are not known at the moment.
Acknowledgements We would like to thank Dr. Joseph Veech (University of Northern Colorado) for his invaluable help, corrections in English and comments on the first draft of this work. Also, Aziz Deveci, Muharrem Balcı, Derya Avuka, and Duygu I˙smailog˘lu from Abant Izzet Baysal University were kindly acknowledged for their continuous help in both field and laboratory studies.
References Akbulut, A., 2003. Planktonic diatom (Bacillariophyceae) flora of Sultan Sazlıg˘ı Marshes (Kayseri). Turk. J. Bot. 27, 285–301. Aykulu, G., Obalı, O., Go¨nu¨lol, A., 1983. Ankara c¸evresindeki bazı go¨llerde fitoplanktonun yayılıs¸ı. Dog˘a Bil. Der. Tem. Bilimleri 7, 277–288. Aysel, V., Gezerler-S¸ipal, U., Aysel, F., Erdog˘an, H., Tu¨rker, E., 2002. Barutc¸u Go¨lu¨’nu¨n (Selc¸uk, I˙zmir, Tu¨rkiye) Mikro-ve Makro-algleri. E.U.J. Fish. Aquat. Sci. 19, 1–11. Buzzi, F., 2002. Phytoplankton assemblages in two sub-basins of Lake Como. J. Limnol. 61, 117–128. Go¨nu¨lol, A., Obalı, O., 1998. A study on the phytoplankton of Hasan Ug˘urlu Dam Lake (Samsun-Turkey). Turk. J. Biol. 22, 447–461. Huber-Pestalozzi, G., 1983. Das Phytoplankton des Su¨ßwassers. 7. Teil: Chlorophyceae (Grunalgen) Ordnung Chlorococcales. In: Elster, H.J., Ohle, W., (Eds.). Band XVI. Die Binnengewasser. Scweizerbart’sche Verlagsbuchandlung, Stuttgart. 1043 pp. John, D.M., Whitton, B.A., Brook, J.A., 2002. The Freshwater algal flora of the British Isles, Ist ed. Cambridge University Press, Cambridge, p. 702. Kılınc¸, S., 1998. A study in the seasonal variation of phytoplankton in Hafik Lake (Sivas, Turkey). Turk. J. Bot. 22, 35–41. Kitner, M., Poulickova, A., 2003. Littoral diatoms as indicators for the eutrophication of shallow lakes. Hydrobiologia 506–509, 519–524. Kovach, W., 1998. Multi-Variate statistical package. Ver.3.01. Pentraeth. Krammer, K., Lange-Bertalot, H., 1991a. Bacillariophyceae. 3. Teil: Centrales, Fragilariaceae, Eunotiaceae. In: Ettl, H., Gerloff, J., Heynig, H., Mollenhauer, D. (Eds.), (Hrsgb.), Su¨ßwasserflora von Mitteleuropa. Band. 2. Fischer Verlag, Stuttgart, pp. 576. Krammer, K., Lange-Bertalot, H., 1991b. Bacillariophyceae. 4. Teil: Achnanthaceae. Kritische Erganzungen zu Navicula (Lineolatae) und Gomphonema. In: Ettl, H., Gartner, G., Gerloff, J., Heynig, H., Mollenhauer, D., (Eds.), (Hrsgb.), Su¨ßwasserflora von Mitteleuropa. Band. 2. Fischer Verlag, Stuttgart, pp. 437. Krammer, K., Lange-Bertalot, H., 1999a. Bacillariophyceae. 1. Teil: Naviculaceae. In: Ettl, H., Gerloff, J., Heynig, H., Mollenhauer, D., (Eds.), (Hrsgb.), Su¨ßwasserflora von Mitteleuropa. Band. 2. Akademischer Verlag Heidelberg, Berlin, pp. 876.
A. C ¸ elekli, O. Ku¨lko¨ylu¨og˘lu / Ecological Indicators 7 (2007) 497–503 Krammer, K., Lange-Bertalot, H., 1999b. Bacillariophyceae. 2. Teil: Bacillariaceae, Epithemiaceae, Surirellaceae. In: Ettl, H., Gerloff, J., Heynig, H., Mollenhauer, D., (Eds.), (Hrsgb.), Su¨ßwasserflora von Mitteleuropa. Band. 2. Akademischer Verlag Heidelberg, Berlin. pp. 596. Ku¨lko¨ylu¨og˘lu, O., 2004. On the usage of ostracods (Crustacea) as bioindicator species in different aquatic habitats in the Bolu region, Turkey. Ecol. Indicators 4, 139–147. Nygaard, G., 1949. Hydrobiological studies on some Danish ponds and lakes. Det Kongelige Danske Videnskabernes Selskab VII, 3–265. Pfiester, L. A., Popovsky, J., 1990. Dinophyceae (Dinoflagellida). In: Ettl, H., Gartner, G., Gerloff, J., Heynig, H., Mollenhauer, D., (Eds.), (Hrsgb.), Su¨ßwasserflora von Mitteleuropa. Band. 6. Fischer Verlag, Stuttgart, pp. 88–218. Potapova, M., Charles, D.F., 2003. Distribution of benthic diatoms in US rivers in relation to conductivity and ionic composition. Freshwater Biol. 48, 1311–1328.
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Prescott, G.W., 1982. Algae of The Western Great Lakes Area. Otto koeltz Science Publishers, W. Germany, pp. 977. Rey, P.A., Taylor, J.C., Laas, A., Rensburg, L., Vosloo, A., 2004. Determining the possible application value of diatoms as indicators of general water quality: a comparison with SASS 5. Water S. A 30, 325–332. Round, F.E., 1981. The Ecology of the Algae. Cambridge University Press, Cambridge, pp. 553. S¸ahin, B., 2000. Algal flora of Lakes Aygır and Balıklı (Trabzon, Turkey). Turk. J. Biol. 24, 35–45. ter Braak, C.J.F., 1995. Ordination. In: Jongman, R.H.G., Ter Braak, C.J.F.,Van Tongeren, O.F.R. (Eds.),Data Analysis in Community and Landscape Ecology. Cambridge University Press, Cambridge, pp. 91–173. Wehr, J.D., Sheath, R.G., 2002. Freshwater algae of North America: Ecology and Classification. Academic Press, California, pp. 918. Youngman, R.E., 1978. Measurement of Chlorophyll-a. Water Research Center, Tech. Rap. Tr-82.
Short Communication
On the relationship between ecology and phytoplankton composition in a karstic spring (C ¸ epni, Bolu) Abuzer C¸elekli, Okan Ku¨lko¨ylu¨og˘lu * Department of Biology, Faculty of Arts and Science, Abant I˙zzet Baysal University, Go¨lko¨y, TR-14280 Bolu, Turkey Received 23 March 2005; received in revised form 10 February 2006; accepted 23 February 2006
Abstract The phytoplankton assemblages and their relationship to physico-chemical environmental variables were studied in Akkaya spring, a limnocrene type of karstic spring pool, for 14 months from May 2003 to July 2004. A total of 63 taxa, belonging to Bacillariophyta (62%), Chlorophyta (29%), Cyanophyta (3%), Pyrrophyta (3%), Euglenophyta (2%), and Chrysophyta (2%), were found. According to CCA analysis, three environmental variables (conductivity, calcium, and sulphate) had the greatest influence on species composition. Based on their seasonal occurrence, most of the species found closer to the center of CCA diagram had cosmopolitan characteristics, while members of the genus Spirogyra were found together in the fall season. Similar seasonal patterns were also recorded in three other crustacean taxa including Cladocera (Daphnia sp.), Copepoda (Cyclops sp.), and Ostracoda (Fabaeformiscandona fabaeformis). Overall, the first two axes of CCA explained 97% of the relationship between species composition and environmental variables. This result was also supported by UPGMA analysis, where three main groups were clustered based on their binary data and ecological preferences. Although physico-chemical characteristics of the pool changed in the following months, after building of a concrete wall around the pool in October 2003, the long-term effect of such changes are not known at the moment. # 2006 Published by Elsevier Ltd. Keywords: Phytoplankton; Ecological indicators; Karstic spring; CCA; Phenology; Bolu
1. Introduction Phytoplankton compositions are affected by different environmental factors such as pH, light, and temperature (Buzzi, 2002). Besides their importance as the primary producers in food webs and ensuring * Corresponding author. Tel.: +90 374 254 1226; fax: +90 374 253 4642. E-mail address: [email protected] (O. Ku¨lko¨ylu¨og˘lu). 1470-160X/$ – see front matter # 2006 Published by Elsevier Ltd. doi:10.1016/j.ecolind.2006.02.006
ecological balance, species of phytoplankton can be useful indicators of water quality (Kitner and Poulickova, 2003; Rey et al., 2004). Although their capacity as indicator species is commonly recognized in the literature, there are few studies from Turkey. Limnological studies have gained momentum in Turkey in the last decades (e.g. Aykulu et al., 1983; Go¨nu¨lol and Obalı, 1998; Aysel et al., 2002) but far from completion. Most of these studies are based on taxonomic levels above species, but few include
A. C ¸ elekli, O. Ku¨lko¨ylu¨og˘lu / Ecological Indicators 7 (2007) 497–503
498
ecological data at the species level. Except some of the earlier studies on ostracods (Ku¨lko¨ylu¨og˘lu, 2004), there is no study focusing on phytoplankton assemblages in the karstic springs of Turkey. Akkaya spring is one of them, known for its special condition in which water quality and plankton composition seem to be affected by interactions of several chemical components. The purpose of this study was to investigate ecological determinants of phytoplankton composition and their seasonal occurrence in Akkaya spring.
for the identification of non-diatom phytoplankton species. We used canonical correspondence analysis (CCA) to determine the relationships between phytoplankton composition and physico-chemical environmental variables (ter Braak, 1995). A cluster analysis of unweighted pair group mean averages (UPGMA) was applied to discern different taxonomic assemblages among the species. All statistical analyses were conducted using the Multi-Variate Statistical Package (MVSP) program version 3.1 (Kovach, 1998).
2. Materials and methods 3. Results 0
0
Akkaya (C¸epni) spring (318, 31 E, 408, 40 N), 17 km southwest of the Bolu, Turkey is a karstic limnocrene spring located at about 1266 m above sea level (Fig. 1). Monthly samples of phytoplankton were obtained from May 2003 to July 2004 for about 14 months. Five environmental variables were measured in situ by using YSI-85 model oxygen-temperature meter, and pH and redox potential were determined using Hanna model HI-98150 pH/ORP meter. Atmospheric temperature and rainfall values were obtained from Bolu Meteorological Station. Chlorophyll-a concentrations were determined by spectrophotometry after extraction in 90% methanol (Youngman, 1978). Standard methods were used to determine chemical analysis. The taxonomic keys of Krammer and LangeBertalot (1991a,b, 1999a,b) were used for diatom identification, while Prescott (1982), Huber-Pestalozzi (1983), Pfiester and Popovsky (1990), John et al. (2002), and Wehr and Sheath (2002) were followed
Fig. 1. Study site located in the city Bolu, Turkey.
A total of 63 taxa (Table 1), belonging to six divisions Bacillariophyta (62%), Chlorophyta (29%), Cyanophyta (3%), Pyrrophyta (3%), Euglenophyta (2%), and Chrysophyta (2%) were found between May 2003 and July 2004. Among the taxa, Asterionella formosa, Fragilaria capucina, Caloneis silicula, and Spirogyra longata located close to the center of CCA diagram (Fig. 2) were found almost continuously during this study. Maximum numbers of species were identified in summer season, while minimum numbers were recorded in late autumn season. The first group of UPGMA dendogram (Fig. 3) includes seven taxa (Spirogyra communis, S. dubia, S. majuscula, Spirogyra spa., Spirogyra spx., Cocconeis placentula and Peridinium willei). The five species of Spirogyra were generally observed during late summer and fall months. The second group was composed of eight taxa, five of which (Oscillatoria terebiformis, Trachelomonas sp., Ceratium hirundinella, Fragilaria dilata, and Navicula radiosa) were found in moderately nutrient rich waters during the summer season. The third group includes the remaining 32 species, most of which have cosmopolitan characteristics known for their high levels of tolerance to changes in environmental variables. Additionally, three accompanying zooplankton groups (Cladocera, Copepoda, and Ostracoda) were found from Akkaya spring during this study. A Holarctic ostracod species Fabaeformiscandona fabaeformis was found throughout the study, except in the onset of summer 2001, while the species of Cladocera (Cyclops sp.) and Copepoda were encoun-
A. C ¸ elekli, O. Ku¨lko¨ylu¨og˘lu / Ecological Indicators 7 (2007) 497–503 Table 1 Total of 63 phytoplankton species found during 14 months of sampling. Code numbers are the same used in CCA diagram Code
Species
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52
Achnanthes stolida Achnanthes sp. Amphora ovalis Asterionella formosa Aulacoseria granulata Caloneis silicula Cocconeis placentula Cyclotella planctonica Cymatopleura elliptica Cymbella affinis C. cistula C. helvetica C. silesiaca Fragilaria biceps F. capucina F. construens F. crotonensis F. dilata Gomphonema angustum G. parvulum G. truncatum Navicula clementis N. radiosa N. reinhardtii Nitzschia sigmoidea N. vermicularis Stauroneis sp. Chlamydomonas sp. Geminella sp. Gonatozygon brebissoni G. kinahanii Spirogyra communis S. dubia S. fluvitialis S. longata S. majuscula S. mirabilis Spirogyra spa. Spirogyra spx. S. weberi Ulothrix sp. Oscillatoria tenuis O. terebiformis Trachelomonas sp. Ceratium hirundinella Peridinium willei Dinobryon divergens Cymatopleura solea Epithemia adnata Fragilaria ulna F. ulna var. acus Hantzschia amphyoxys
499
Table 1 (Continued ) Code
Species
53 54 55 56 57 58 59 60 61 62 63
Melosira lineata Navicula trivialis Navicula sp. Pinnularia rupestris Rhopalodia gibba Surirella subsalsa Tabellaria sp. Mougeotia parvula M. scalaris Oocystis sp. Roya sp.
tered all year around in the pool. In total, 97% of the relationship between species and environmental variables was explained by the first two axes of CCA. Conductivity, calcium concentrations and sulphate had the greatest influence on the species assemblages (Fig. 2). Physico-chemical variables changed with season and minimum, maximum and mean values of environmental factor are given in Table 2.
4. Discussion and conclusion Finding total of 63 phytoplankton taxa dominated by Bacillariophyta corresponds to earlier studies done in variety of habitats. Indeed, earlier studies stated that Bacillariophyta was the dominant group in Lake Hafik (Kılınc¸, 1998) and in Lake Aygır and Balıklı (S¸ahin, 2000). Compared earlier research, we also found relatively high percentage of Bacillariophyta among the phytoplankton assemblage. It is known that diatoms are generally a dominant group in calcareous regions (Round, 1981). Therefore, the differences in the species composition are possibly due to the difference in the properties of water where extreme conditions are already present in Akkaya spring. The members of phylum have high tolerance towards chemicals and were also found in different habitats in Turkey (Kılınc¸, 1998; Akbulut, 2003). Most of these diatoms (e.g. Cymbella, as calciphilous taxa) known to tolerate different concentrations of Ca(HCO3)2 were also found in water with a high conductivity (Potapova and Charles, 2003). Indeed, finding some of the species of Cymbella close to the vector of calcium in the CCA diagram (Fig. 2) supports this observation.
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Fig. 2. Diagram of canonical correspondence analysis (CCA) shows 14 months, 47 species, and 12 environmental variables. Abbreviations and species codes (numbers) are shown in following Table 1.
During the study period, some species such as A. formosa, F. capucina, and S. longata were found almost all year around. Species richness was increased during summer months, while it decreased during late fall and winter months. It can be consequence of decreasing in water temperature. However, CCA diagram failed to show this effect (Fig. 2). The most diverse genus was Spirogyra (with nine species), most of its members are usually restricted to hard waters. Spirogyra is generally found in soft, slightly acidic waters rich in organic acids. However, some Spirogyra species as seen in our case can also be found in extreme conditions. For example, S. communis was common in the fall season in Akkaya spring. This suggests that the species prefers nutrient rich, calcareous, and slightly acidic waters (John et al., 2002). A. formosa, which was the most common diatom in fall and especially in spring months, has been reported as dominant species even in eutrophic lakes (Nygaard, 1949). Although this species has a high tolerance to extreme water chemistry, its occurrence may be related to its specific phenological characteristics (Round, 1981). In the present study, A. formosa was dominant in April and May 2004 when
phosphate concentrations of the spring water were maximized. CCA analyses suggested that the majority of phytoplankton species have substantial tolerance to different environmental variables. Indeed, among 47 phytoplankton taxa used in the CCA analyses, 24 of them were close to the center of the CCA diagram. This is probably due to the cosmopolitan characteristics of these species (Fig. 2) that indeed, all are known to tolerate large ranges in water qualities. Thus, it seems, overall, phytoplankton assemblage was highly affected by conductivity and calcium concentration (Fig. 2). The dendrogram of UPGMA showed three distinct groups (Fig. 3). In the first one, seven taxa were included (S. communis, S. dubia, S. majuscula, Spirogyra spa, Spirogyra spx, C. placentula, and P. willei). Five species of Spirogyra were generally observed during late summer and fall sampling months. This corresponds with the findings of earlier reports. For example, John et al. (2002) reported that most members of Spirogyra appear in the autumn season and disappear in the summer season. The second clustered group is composed of eight
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Fig. 3. UPGMA dendrogram shows three major clustering groups. Species codes (numbers) are shown in Table 1.
taxa, most of which were reported from moderately nutrient rich waters in the summer months. The third group includes most of the cosmopolitan species located in the center of the CCA diagram (Fig. 2).
Seasonal differences in species composition may be related to rainfall because the amount of rainfall can alter water chemistry including pH. Indeed, the CCA diagram (Fig. 2) showed that rainfall (referring to water precipitation) reflects a negative relationship
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Table 2 The mean, minimum and maximum values of physico-chemical variables measured in Akkaya spring Minimum Maximum Mean Water temperature (8C) 13.9 Air temperature (8C) 1.4 Rainfall (mm) 1.6 Dissolved oxygen (mg/l) 1.93 Saturation (%) 16.2 Conductivity mS/cm 881 Redox potential (Eh) (mV) 5 pH 6.27 Salinity (ppt) 0.4 Turbidity (NTU) 0.2 Chlorophyll-a (mg/l) 0.23 BOD (mg/l) 0.03 HCO3 (meq/l) 23.6 0.009 NO2–N (mg/l) NO3–N (mg/l) 0.006 PO4–P (mg/l) 0.008 NH4–N (mg/l) 0.011 0.26 SO42 (meq/l) Cl (meq/l) 0.69 Ca2+ (meq/l) 25.65
25.1 24.5 97.9 15.5 154.3 2046 41.2 7.76 1 15 7.5 4.05 28 0.046 0.096 0.019 0.115 1.05 10.1 40.01
19.5 12.1 50.9 6.4 69.9 1788 25.6 6.7 0.9 2.1 2.28 1.94 25.7 0.02 0.043 0.01 0.043 0.6 2.88 30.41
n 29 29 29 29 29 29 26 29 29 21 9 12 9 9 6 9 9 9 9 6
with pH and conductivity, but there was a positive relationship between the precipitation and some other variables such as sulphate, nitrite, and phosphate as well. Increasing precipitation seems to cause a decrease in pH level that eventually increases calcium dissolution in the water, which may cause a change in species composition. For example, Cymbella and Achnanthes, which can tolerate such extreme conditions, are known as calciphiles or calcium loving organisms. Consequently, precipitation may have also an important effect on species composition in Akkaya spring. Additionally, anthropogenic factors also play an important role on the habitat structure and species composition in Akkaya spring. Because of its relatively warm water, the area is open for human use such as swimming, bathing, and picnicking. Because of increasing demand by the cities populace, a concrete wall was built around the spring to collect water in a pool. After building this artificial structure, water composition of the spring changed. This action caused some of the species (i.e. F. fabaeformis, a bottom dependent ostracod inhabiting shallow habitats) to disappear from the area. Similar changes were observed in the phytoplankton community in short term, but the long-term effects are not known at the moment.
Acknowledgements We would like to thank Dr. Joseph Veech (University of Northern Colorado) for his invaluable help, corrections in English and comments on the first draft of this work. Also, Aziz Deveci, Muharrem Balcı, Derya Avuka, and Duygu I˙smailog˘lu from Abant Izzet Baysal University were kindly acknowledged for their continuous help in both field and laboratory studies.
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