Issue |
Int. J. Lim.
Volume 58, 2022
|
|
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Article Number | 3 | |
Number of page(s) | 12 | |
DOI | https://doi.org/10.1051/limn/2022002 | |
Published online | 19 May 2022 |
Research Article
Determining effective environmental factors and ecology of non-marine Ostracoda (Crustacea) in Giresun, Turkey
1
Department of Biology, Balıkesir University, Balıkesir, Turkey
2
Department of Biology, Faculty of Arts and Science, Bolu Abant İzzet Baysal University, 14280 Bolu, Turkey
3
Institute of Geology and Mineralogy, University of Cologne, 50674 Köln, Germany
* Corresponding author: kulkoyluoglu_o@ibu.edu.tr
Received:
22
April
2021
Accepted:
22
January
2022
To determine influential environmental factors on ostracod species, 105 aquatic sampling sites were sampled from the Giresun province. Sixteen species collected from 69 sites are new records for the study area. Seven of 16 species were found in their expected geographical distribution while two species (Ilyocypris bradyi, Psychrodromus olivaceus) showed different distribution (P < 0.05). Of which, P. olivaceus displayed a limited distribution in the northern region of the study area. Geographical distribution of some species and their co-occurrences varied among habitats. The mean values of three variables (water temperature, electrical conductivity, and elevation) were significantly different in northern region than the values of the sampling sites in the southern region (P < 0.01). Canonical Correspondence Analysis explained 72.5% of the significant relationship (P < 0.05) between species and four most effective environmental variables (water temperature, electrical conductivity, elevation, and magnesium). Heterocypris salina and Potamocypris fallax exhibited maximum and minimum tolerance (and optimum) values for electrical conductivity, respectively. Heavy metal presence on the carapace surfaces was investigated using Energy Dispersive X-ray Analysis (EDX) along with SEM photographing. The observation of metals such as copper, aluminum, silver and even radioactive element such as technetium on the carapace surfaces suggests that the organisms studied actually carry much more information about their aquatic environment than it was thought. Overall, our results support the findings of previous studies that water temperature and electrical conductivity were the two most effective factors on ostracod species and can be responsible for their distribution and occurrences in sampling area.
Key words: Ecological tolerance / effective factors / ostracoda / distribution / diversity
© EDP Sciences, 2022
1 Introduction
Nonmarine ostracods can survive in almost all kinds of aquatic habitats (e.g., springs, creeks, lakes, ponds, ditches, canals, reservoirs, peat moss and underground waters) from sea level to above 5000 m a.s.l. Also, several species are known from interstitial habitats. Among the 15 different freshwater taxonomic groups (i.e., classes) of Crustacea, following Copepoda (Balian et al., 2010), ostracods are the second-largest nonmarine group with about 2330 subjective species (Meisch et al., 2019). By contrast to other crustaceans, ostracods have several other important biological and ecological characteristics including relatively short reproductive periods (e.g., see Van Doninck et al., 2003; Külköylüoǧlu et al., 2012c), large clutch size (Gandolfi et al., 2001), short developmental stages (Cohen and Morin, 1990), high dispersal ability (passive or active dispersion) (Dole-Olivier et al., 2001), presence of desiccation-resistant eggs (Horne, 1993), relatively high tolerance levels to different environmental variables (Akdemir et al., 2016), and having both sexual and asexual (and/or mixed) populations. Besides, ostracods with their global distribution in a variety of freshwater and marine aquatic systems have very old fossil records going back to the Cambrian period (Williams et al., 2008).
Freshwater ostracods are suitable bioindicators because they have a certain level of tolerance to some environmental variables (Benson, 1990; Delorme, 1991; Külköylüoğlu, 1999; Ruiz et al., 2013). Studies have reported possible correlations between the occurrence patterns and distribution of the species with different environmental (e.g., water temperature, salinity, dissolved oxygen) (Mezquita et al., 2001; Wansard and Mezquita, 2001), biological (e.g., presence of macrophytes, competition, and predation) (van Varten, 1983), and geogra-phical variables (e.g., elevation, temperature) (Horne and Boomer, 2000; Külköylüoğlu, 2005a; Pérez et al., 2010). Ostracods are useful indicators for determining environmental changes (Wise, 1961; Ruiz et al., 2004). Based upon the shape, size, and ornamentation, ostracods can be used as tools for describing past environmental conditions (Wise, 1961; Benson 1990). All ostracods possess two calcium carbonate valves (carapace) linked to each other medio-dorsally by a hinge structure. The carapace consists almost entirely of calcium carbonate contents (Turpen and Angel, 1971; Chivas et al., 1986, but see discussion in Keyser and Walter, 2004). As a consequence, their calcitic valves readily preserve as fossils. Although Ca is a dominant element in the carapace, some other elements (e.g., magnesium, strontium, sodium, phosphate, etc.) also occur in trace amounts. On the other hand, presence of trace elements on carapace is important issue because toxic effect of heavy metals can influence ostracod populations (Ruiz et al., 2004; Khangarot and Das, 2009; Shuhaimi-Othman et al., 2011). Species gain these elements directly from the aquatic environment they inhabit (Turpen and Angel, 1971; Palacios-Fest et al.1994; Wansard et al., 1999). Since individual species represent the characteristics of waters in which they live, detection of those elements on carapace aids to understand characteristics of water quality, implying to understand past historical aquatic conditions. This refers to seek a possible relationship between carapace and chemical composition of the water which can be one of the influential factors on species occurrences.
Ostracods can be distributed evenly over long distances through passive or active transportation (Danielopol et al., 1994). In passive mode, adults or eggs are transported by different factors such as wind, some plants, insects, amphibians, fishes, birds and humans (Horne et al., 1998; Külköylüoğlu, 1999; Meisch, 2000, Rossi et al., 2003; Valls et al., 2016). The length of swimming setae can provide more efficient mobility of the ostracods active transport. Although ostracods have wide geographical distributional ranges along with many different habitat types, which environmental factor(s) can be a better predictor for their distribution is not well understood. Accordingly, the aims of the present study are to (i) contribute knowledge into the ostracod fauna of the Giresun province, (ii) assess the correlation between the most effective ecological variables on individual species along with calculating their ecological optimum and tolerance values, (iii) detect trace elements or heavy metals on the carapace, and (iv) observe distributional patterns of ostracods across the aquatic habitats of the province.
2 Materials and method
2.1 Area description
Giresun (40° 07'- 41° 08' N 37° 50'- 39° 12' E, 6934 km2 in surface area) is in the Eastern Black Sea region of Turkey. The northern part of the area is bordered by 105 km of the Black Sea coast. At the same time, a fairly rugged Giresun Mountain range bound the south side (ca. 2000 m a.s.l.), which extend 50 to 60 kilometers from the shoreline of the sea. Two different types of climates characterize the area under the influence of the Giresun Mountains. One of them occurs in the northern part, marked as warm and with rainy conditions. The other with a continental climate is the Kelkit Basin at the southern part. The eastern Black Sea region has a relatively long rainy period. Hence, the lowest and highest temperature fluctuations varied from February (–9.8 °C) to October (37.30 °C) between 1929 and 2018, with total annual rainfall was of ∼1288 mm/yr (107.33 mm/month) (Turkish State Meteorological Service, 2019). Karakaya et al. (2007) and Karakaya and Çelik Karakaya (2014) provide a detailed information on the chemical characteristics of more than 40 different aquatic systems (i.e., spring, rivers, streams, and drainage waters) in the Giresun province (note that they sampled the area in 1996 and 1997, and their sites were different than ours sampled during the present study). According to their results about the water quality of the province, it was indicated that most of these water bodies were acidic (pH 1.85–8.53) in average of 5.20 with high sulfate content, and even in some cases, concentrations of Pb, Zn, Fe, and Cu was found in extreme levels (Karakaya et al., 2007; Karakaya and Çelik Karakaya, 2014). Besides, the authors listed above also underlined that levels of some elements (e.g., Cd, As, Mo, Se, Sb, Tl, Bi) occurred above the levels of acceptable (inter)national drinking water limits. Due to these high metal levels and pollution values, there can be a great environmental risk for life in these waters (Karakaya and Çelik Karakaya, 2014; pers. comm. to Karakaya, N). The waters studied by these authors are mostly acidic, low in dissolved oxygen (average 6.98 mg/L), and relatively cold waters (average 19.68 °C) with a high average value of EC (1838.3 mS/cm). Note that this high EC value might be due to the characteristics of the drainage systems (see Tab. 1 in Karakaya and Çelik Karakaya, 2014).
Comparison of the habitat types in the Giresun province with collected ostracods.
2.2 Sampling
In total, 105 water (Fig. 1) and sediment samples were randomly collected from different shallow (ca. 100 cm of depth) aquatic bodies during the period of 3–8 October 2015. Sampling included nine different aquatic habitats such as lake, creek, trough (man-made artificial container), ditch, stream, plunge pool of waterfall, river, pond and pool. Ostracod samples collected with a hand net (200 µm mesh size) from sediment (ca. 5 cm of depth) and open water were preserved in 70% ethanol in 250 ml plastic bottles. About 100 ml of water samples were also kept in clean plastic bottles for chemical analyses. All samples were saved at 4 °C in ice chests. Raw sediment samples were collected in Eppendorf vials for chemical analysis. After the field study, each ostracod sample was filtered with three-layer sieves (200, 150, 100 μm mesh size) in the laboratory under tap water and kept in 70% ethanol. We used needles to separate ostracods from sediment under a stereomicroscope (Olympus ACH 1X). Adult individuals were dissected in lactophenol solution for taxonomic identification. We followed the taxonomic keys of Meisch (2000) and Karanovic (2012) for species identification with the aid of a light microscope (Olympus BX-51). Using a JEOL JSM-6390LV Scanning Electron Microscope (SEM), photomicrographs of gold coated (4 μA) single valves were used. Valves werecoated them with a COXEM KIC IA model ION COATER. With the Energy Dispersive X-Ray Analyzer installed in the SEM, chemical composition of single valves of one individual per species was identified. All ostracod samples were stored at the Limnology Laboratory of Bolu Abant İzzet Baysal University, Turkey, and can be available upon request from the corresponding author.
In the field, we used a YSI-Professional Plus device to measure dissolved oxygen concentration (DO, mg/L), percent oxygen saturation (% sat.), water temperature (Tw, °C) electrical conductivity (EC, µS/cm), total dissolved solids (TDS, mg/L), salinity (Sal, ppt) pH, atmospheric pressure (mmHg). To obtain the meteorological data (wind speed (km/h), air moisture (%), air temperature (Ta, °C), at each sampling site, we used a Testo 410-2 anemometer. The site coordinates and elevation (m) were obtained using a Garmin e-Trex Vista H GPS. Furthermore, we analyzed water samples with the standard method (no: 4110) using Ion Chromatography (Dionex 1100) to calculate cations and anions of the sampled waters at the Department of Environmental Engineering, Bolu Abant İzzet Baysal University. Sodium (Na2+), potassium (K2+), magnesium (Mg2+), calcium (Ca2+), fluoride (F–), chloride (Cl–), nitrite (NO2 –), nitrate (NO3 –) and sulfate (SO4 2–) characterized the water samples associated with organic and inorganic phosphate (PO4 3–) from the sediments measured in parts per million (ppm).
Fig. 1 Total of 105 randomly selected sampling sites (numbers shown on the map from 1 to 105) from 16 counties (Merkez, Alucra, Bulancak, Çamoluk, Çanakçı, Dereli, Doğakent, Espiye, Eynesil, Görele, Güce, Keşap, Piraziz, Şebinkarahisar, Tirebolu, Yağlıdere) of the Giresun province, Turkey. |
2.3 Statistical analyses
Using a Normality test, we calculated the ostracod species abundances (numbers of individuals per site). For this reason, we ran a one-sample Kolmogorov-Smirnov Z test for nine of the most frequently occurring species in the SPPS program (version 20.0). The C2 program calculated ecological optimum (uk) and tolerance (tk) levels of ostracod species encountered from three or more locations. Also, using the C2 software, we conducted the transfer function of weighted averaging regression (Juggins, 2003). Besides, as a multivariate statistical method, Canonical Correspondence Analysis (CCA) with a 499 Monte Carlo Permutation test was applied to detect possible relationships among ostracods and ecological variables. CCA was also used to portray the most effective environmental variable(s) on the ostracod species distributed among the sampling sites. The compatibility of the data for CCA was applied to log-transformation and then tested with DCA (Detrended Correspondence Analysis). Accordingly, values of DCA higher than three are convenient for CCA handling (ter Braak, 1987; Birks et al., 1990). DCA values equal or greater than 3 are a sign that species fit the full Gaussian distribution. To minimize the arc-effect and eliminate the multicollinearity, we removed CCA values of species with rare occurrences and variables with a highly influential factor in the analyses. In the summary, larger eigenvalues of the first two axes offer a good explanation of the data (Birks et al., 1990). The diagrams show the position of each variable and species analyzed across the sampling sites. It displays the correlations among the variables, species, and sites.
3 Results
A total of 16 ostracod species (Neglecandona neglecta (Sars, 1887), Cypridopsis vidua (O.F. Müller, 1776), Herpetocypris reptans (Baird, 1835), He. intermedia Kaufmann, 1900, Heterocypris incongruens (Ramdohr, 1808), Ht. salina (Brady, 1868), Ilyocypris bradyi Sars, 1890, I. brehmi Schäfer, 1952, I. inermis Kaufmann, 1900, Potamocypris fallax Fox, 1967, Po. fulva (Brady, 1868), Po. villosa (Jurine, 1820), Pseudocandona albicans (Brady, 1864), Psychrodromus fontinalis (Wolf, 1920), P. olivaceus (Brady & Norman, 1889), Scottia pseudobrowniana Kempf, 1971) occurred in 69 of 105 locations in the Giresun province. All species (Supplementary Material - Fig. S1) reported here are new records for the area. Ilyocypris bradyi was the most common species presented in 17 locations, followed by P. fontinalis (16 sites) and four other species (P. olivaceus, Ht. incongruens Po. fallax, Po. villosa) occurred in 15 sites (Fig. 2, Tab. S2). The most diverse sampling site was a trough with six species. Results indicated that the distribution of P. olivaceus was limited to the sampling sites distributed in the northern parts of the province (Fig. 3). The northeastern portion of the area of study did not contain ostracods, whereas the highest diversity occurred in the central and southern areas (Fig. 3). The two most common species found together from seven stations are Ht. incongruens and Po. villosa. During field work, we observed that the probability of finding a site without ostracods was somewhat 35% (69 sites with ostracods from 105 sites). In contrast, the ratio of finding ostracods was relatively high (90%) in the troughs (Tab. 1).
Canonical Correspondence Analysis (CCA) explained 72.5% of variations between the relationships of nine species and four ecological variables (Tab. 2). CCA diagram (Fig. 2) showed that four variables (Tw (F = 3.044, P = 0.003), EC (F = 3.995, P = 0.007), Elev (F = 2.845, P = 0.008), Mg (F = 3.672, P = 0.019)) displayed significant correlation to the species while three other variables (Ca (F = 2.137, P = 0.081), DO (F = 1.095, P = 0.336), pH (F = 0.943, P = 0.453)) did not show significant relationships with them. Among the species, N. neglecta showed a high positive correlation with elevation but Ht. Salina displayed a positive correlation with Mg and EC. Individual species revealed different levels of tolerance and optimum values for different environmental variables (Tab. 3). Both Ht. salina and Po. fallax displayed maximum and minimum tolerance and optimum values for EC. By contrast, N. neglecta and Po. villosa had minimum optimum and tolerance levels for EC, respectively. The maximum tolerance level for water temperature was found for P. fontinalis when Po. fallax exhibited minimum tolerance and optimum estimates for the temperature. In contrast, P. olivaceus indicated the highest optimum value for Mg when N. neglecta has a maximum level of tolerance. Measured elements of the carapace by EDX revealed the presence of 15 different elements (O, C, Ca, Mg, Na, Sr, P, Cu, Rb, Al, Si, S, Tc, Ar, Ag) on the 17 ostracod valves (Tab. S1). As expected, three elements (O, C, and Ca) made up about 98% of the carapace structure (Tab. 4). Silver was found in the P. olivaceus valve while copper was found in the Ht. incongruens valve, and aluminum was in the I. bradyi and C. vidua. Moreover, as far as we know, this is the first time that trace amount of technetium (Tc) was encountered in the Ps. albicans valve. Our results following the known literature (41 ecology-related studies) revealed that water temperature and electrical conductivity (Tab. 5, Tab. S1) are the most critical factors responsible for ostracod species distribution and occurrences in the present study.
Fig. 2 The CCA diagram indicates the relationship between four ecological variables (water temperature (Tw), the magnesium content of water (Mg), elevation (Elev), electrical conductivity (EC)) and nine species (Neglecandona neglecta (NN), Ht. incongruens (HI), Ht. salina (HSa), I. bradyi (IBr), Po. fallax (PF), Po. fulva (PFu), Psychrodromus olivaceus (PO), P. fontinalis (PFo), Po. villosa (PVi)) from 64 different sampling sites in the Giresun province. |
Fig. 3 Distribution of ostracod species (Psychrodromus olivaceus, Potamocypris fulva) in the Giresun province. Empty sites simply “absence of ostracods”. |
CCA summary table with four variables (electrical conductivity, magnesium, nitrate and water temperature) and nine species with three or more times occurrences from the Giresun province (*DCA results).
Tolerance (Tol) and optimum (Opt) values for the nine most common species against the variables measured from each sampling site. Abbreviations: Count (numbers of species occurrence), Max (maximum numbers of individuals), N2 (Hill's coefficient or measure of effective number of occurrences), dissolved oxygen (DO, mg l−1), electrical conductivity (EC, μS cm−1), water temperature (Tw, °C), redox potential (ORP), elevation (Elev), sodium (Na2+, ppm) in water, magnesium (Mg2+, ppm) in water, calcium (Ca2+, ppm) in water, fluoride (F–, ppm) in water, chloride (Cl–, ppm) in water, total phosphate (T.PO4 3–, ppm) in sediment.
Elemental atomic percentage (%) values from the carapace surface of 17 ostracod species according to EDX analyses. Elements found in trace amounts are listed under ‘Others’. Numbers written in parentheses indicate the number of sampling site.
A) Mean, minimum (Min) and maximum (Max) values of environmental, and B) chemical variables measured from the sampling sites. Abbreviations: DO, dissolved oxygen; EC (electrical conductivity); Tw (water temperature); Atmp (atmospheric pressure); ORP (oxidation-reduction potential); elevation (Elev); Sal (salinity); TDS (total dissolved solids); sodium (Na2+); chloride (Cl–); magnesium (Mg2+); calcium (Ca2+); nitrite (NO2 –); nitrate (NO3 –); sulphate (SO4 2 –); total phosphate T.PO4 3 –. (*) eight meters below the sea level. Ion values are in ppm.
4 Discussion
4.1 Species occurrences and diversity
Previously, seven ostracod species (Potamocypris steueri, Xestoleberis aurantia aurantia, Loxoconcha rhomboidea, Paradoxostoma guttatum, Callistocythere mediterranea, Pontocythere baceseoi, Eucytherura bulgarica) had been reported from the Turkish province of Giresun (Kılıç, 2001). However, among those species, Po. steueri is the only one belonging to freshwater habitats. In contrast, the remaining species are known to inhabit brackish and/or marine waters along the Black Sea coasts. During the present study, Po. steueri did not occur in the area of study. To date, 17 species of nonmarine ostracods are known in the area, including Po. steueri. The diversity of species is low when compared to other parts of the region. For example, Erzincan (Akdemir and Külköylüoǧlu, 2014) and Ordu (Külköylüoǧlu et al., 2012c) provinces to the south and west of Giresun include 32 (from 63 of 89 sites) and 26 (from 133 of 166 sites) ostracod species, respectively. This number is even lower than several other reports in other regions of Turkey such as 29 species in Gaziantep (Akdemir et al., 2016), 22 species in Karabük (Külköylüoǧlu et al., 2017) and 22 species in Burdur provinces (Yavuzatmaca et al., 2017a) and elsewhere, for instance, Italy (Pieri et al., 2009). One may consider reasons for finding relatively fewer numbers of ostracods in Giresun. Before providing possible answers, it is important to point out that there were no significant differences in the methodology and sampling methods used in these studies. Besides, the number of sampling sites is also not the main problem since there are already other studies with less and more sampling sites (e.g., see Rossi et al., 2003; Martins et al., 2010; Martínez-García et al., 2015) than the present study. Accordingly, there can be at least three possible reasons for finding comparatively low numbers of species from Giresun. First, the timing of sampling (referring to month or season) may directly reflect on species occurrences. Most ostracods have a defined seasonal occurrence pattern (Lerner-Seggev, 1968; Rieradevall and Roca, 1995). It seems that both autumn and summer seasons in the northern hemisphere favor ostracods more than the spring and winter seasons (Külköylüoğlu, 1998; Akdemir, 2008; Gürer and Külköylüoğlu, 2019). We conducted fieldwork for a few days in the autumn; therefore, a comparison of seasonal differences cannot be considered herein with those of previous works. Indeed, there are other studies (e.g., see Külköylüoǧlu et al., 2017, 2018) that sampled within the same month and/or same season where more species were reported. Second, there can be historical reasons for finding low numbers of species in the province. For this reason, palaeontological studies may provide an answer. However, at present, it is not possible to compare species numbers because there are no palaeontological studies in the area, whereas such studies are known for different regions of Turkey (e.g., see Tunoğlu, 2003; Tuncer and Tunoğlu, 2015; Nazik et al., 2018). Thirdly, the species characteristics, referring to competitive factors of dominant species over non-dominant ones, can be influential. In this case, eight (N. neglecta, Po. villosa, Ht. incongruens, Ht. salina, C. vidua, Ps. albicans, I. bradyi, P. olivaceus) of 16 species reported in the present study are thought to be cosmopolitan (Külköylüoğlu, 2013). Cosmopolitan do have some advantages over noncosmopolitan species. For example, they occur in a wide range of habitats (Mezquita et al., 1999; Meisch, 2000; Martínez-García et al., 2015; Yavuzatmaca, 2019) with wide ranges of tolerance and optimum values for different environmental variables (Külköylüoğlu et al., 2013, 2016, 2018, 2019a, b). Cosmopolitan species have an important effect on species assemblages among the aquatic habitats. They use their selective advantages over noncosmopolitan species to reproduce seasonally and grow faster along with having high tolerance and optimum values for a/biotic factors (Smith and Horne, 2002). Eventually, these species can indeed be useful as beta diversity indicators (e.g., see Nagorskaya and Keyser, 2005) between the areas where they can affect differences in total numbers of species (species diversity). Although we did not provide robust evidence for the effect of cosmopolitan species on total diversity, they were the species with the most frequent occurrences among the sites during the present study.
4.2 The effect of ecological factors on the distribution
Figure 2 portrays CCA results with four variables (Tw, EC, Elev, Mg) found with close relationships with ostracods from the Giresun province. This result coincides with the known studies available in the literature (Tab. S1) that water temperature and electrical conductivity were the two most influential variables controlling ostracods. Indeed, as stated above, out of 42 ecology-based studies, 29 and 22 of them underlined that water temperature and electrical conductivity were the most useful/effective variables, respectively. Besides, according to these studies, pH and elevation were only found valuable in 13 and 11 of them, respectively. However, the influence of these variables on individual species can show differences. For example, Figure 2 clearly illustrates a close correlation between Ht. salina and electrical conductivity and magnesium content (compare the arrows in Fig. 2). Still, some other species are on the opposite side of the arrows. Previous investigations (e.g., Meisch, 2000; Fuhrmann, 2013; Scharf et al., 2016) report Ht. salina from fresh to brackish waters where it can tolerate high levels of salinity values. Pint et al. (2015) clustered this species in waters with high contents of chlorides. In contrast, we found it from the waters with a high concentration of Ca and SO4 2–with a relatively low (8.9 °C) to medium (19.7 °C) temperature ranges. However, it was collected in warm waters with year-round temperature of 26 °C (Külköylüoǧlu et al., 2013) or even up to 34 °C (Pax 1942, 1948).
Similar to Ht. salina, Ilyocypris bradyi, the most common species responding to a wide range of variables thrives in almost all types of aquatic bodies (Pieri et al., 2009; Li et al., 2010). The correlation between the two species was positive (P < 0.05). Ilyocypris bradyi is a non-swimmer benthic ostracod, but Ht. salina can swim. This may explain finding a positive correlation between the two species since Ht. salina can swim and change its location in a water body when I. bradyi prefers bottom. Differences in mobility and microhabitat preferences may eliminate competitive interaction between these two cosmoecious species (Külköylüoğlu, 2013). In contrast, Ht. incongruens, another well-known cosmoecious species (Külköylüoğlu, 2013) is on the opposite side on the CCA diagram. This species lives in a variety of waters with high ranges for salinity (3320 μS/cm) (Mezquita et al., 1999), temperature (31.7 °C) (Külköylüoğlu, 2013), and low oxygen (1.0 mg/l) (Külköylüoğlu, 1999) levels (also see Yavuzatmaca and Külköylüoǧlu, 2019). However, the fact that Ht. incongruens tolerates wide ranges of ecological variables amid shallow aquatic bodies with specific amounts of phosphate components (Pint et al., 2015; Yavuzatmaca and Külköylüoǧlu, 2019). Our study supports the hypothesis that the species has very high optimum levels for total phosphate. Similar to Ht. incongruens, two other cosmoecious species (N. neglecta and Po. villosa) occur on the left side of the diagram (Fig. 2). Neglecandona neglecta is closer to the arrow of elevation on the diagram while Po. villosa is far above it. These species are of similar cosmoecious characteristics which are widely distributed among different types of aquatic habitats where they are also known to tolerate a variety of aquatic conditions (Külköylüoğlu, 2013). Pint et al. (2015) did not find Ht. incongruens and C. vidua in waters with high Ca contents and underlined that their absence could indicate such waters in studies aiming to reconstruct past historical conditions. Although C. vidua was found from two different habitats during our research, in both cases, the species was found from Ca and SO4 2–-dominated waters. Supporting evidence to these findings comes from the study of Peterson et al. (2013). They found live specimens of C. vidua from the Frasassi sulfidic spring adjacent to the Frasassi Caves system in northeastern Apennines of Italy. These results suggest that C. vidua has some levels of tolerance in waters enriched in sulfate contents. Several studies reported C. vidua from low (37 μs/cm) (Meisch and Broodbakker, 1993) to high levels of salinity (7410 μs/cm) (Meisch et al., 2007) where it can tolerate low oxygen levels (Külköylüoğlu, 2003; Martins et al., 2010).
Psychrodromus olivaceus thrives in freshwater habitats, including springs, creeks, ponds, troughs, and slightly flowing zones of streams. Similar to C. vidua, the species was initially encountered in Ca and SO4 2–rich waters, but it can also be found in waters with medium Mg and Cl concentrations. For example, in a monthly study focusing on the association between the chemical structure of ostracod valves and the environmental variables, P. olivaceus accompanied with Po. similis was studied all year-round in a cold (water temperature 9.6–10.7 °C), slightly alkaline (pH 7.11–7.75) freshwater (EC 190.2–342 414 ms/cm) rheocrene spring in Turkey (Külköylüoğlu et al., 2015).
Pseudocandona albicans is another cosmopolitan species, but we did not use the species in correlation analyses due to its single occurrence. Nevertheless, it is a benthic species that is mostly be encountered in the cold to warm springs, creeks, streams, and ponds (Meisch, 2000), as well as in the association of riparian habitats (Iglikowska and Namiotko, 2012). As shown above, although these eight individual species bear typical cosmopolitan characteristics, their levels of tolerance and optimum values vary among the habitats at different elevational ranges. We also found elevation (and temperature) to be one of the four essential variables on species distribution. However, previous studies have reported argumentative results about the effect of elevation/temperature. While some studies (e.g., Mezquita et al., 1999; Pieri et al., 2009) argued that elevation is an influential factor on ostracods, other authors (Laprida et al., 2006; Külköylüoǧlu et al., 2012c; Guo et al., 2013; Yavuzatmaca et al., 2015, 2018) did not support this view. However, current studies (see discussion in Yavuzatmaca et al., 2018) indicated that elevation indirectly play as a secondary role in ostracod distribution and dispersion. Future studies are needed to find more solid evidence for the relationship between altitude and ostracod species distribution and occurrences.
Psychrodromus fontinalis, the second most common species with 16 sampling sites throughout the present study, is a common species with a high tolerance range for environmental factors. This is why it has been observed in six different habitat types. We do not know much about the 13 ecological characteristics of this species, but it is usually reported from springs, waters related to springs, and subterranean waters (Meisch 2000). Most recently (Külköylüoğlu et al., 2020), P. fontinalis was reported from springs where the species showed highest optimum value for redox potential (opt = 82.17) and lowest values for pH (opt = 7.55) and water temperature (opt = 14.23). During the present study, the species thrived in a relatively cold creek (9.1 °C) and trough waters (17.8 °C) where average Ca (41.37 ppm), and Mg (33.01 ppm) values were also relatively high.
In comparison with the other species, I. bradyi has a “thick” and ornamented carapace and is known to tolerate a variety of ecological variables (Yavuzatmaca et al., 2017a, b). For example, according to Bunbury and Gajewski (2005), I. bradyi, referring waters with high Mg/Ca contents, also showed high tolerance for the amount of sodium (ca. 12 mg/l) (see details in their Fig. 6) in the waters. Our study does not support Bunbury and Gajewski's research, and we found that the species from a variety of waters showed a wide range of tolerances to calcium and water temperature (Tab. 3). The content of Na in Ht. salina and He. intermedia is greater than that of other species. Considering the information gained from the previous studies (Karakaya et al., 2007; Karakaya and Çelik Karakaya, 2014), it can be assumed that most of the waters studied in the region are rich in SO4 2–. As indicated above (Tab. 5), Ht. salina was found from Ca and SO4 2–-dominated waters during this study. This occurrence may be a coincidence as shown by other species found in waters with different chemical contents. However, if this is true, it can be useful to apply it in palaeontological studies on fossil ostracod valves such as Ht. salina which has been frequently reported from different regions of Turkey (Tunoğlu, 2003; Tuncer and Tunoğlu, 2015; Nazik et al., 2018). Thus, knowledge about carapace chemistry may aid to estimate past aquatic conditions (Ito et al., 2003) since species prefer certain kinds of waters (Akdemir et al., 2016).
Species, like Ht. salina, can usually be found as fossil due to their well calcified (i.e., calcite crystals) carapaces (Keyser and Walter, 2004). Keyser and Walter (2004) indicate that organisms with a poorly calcified carapace do not produce crystallites. In such a case, they may not be found as fossils because the amorphous calcite is not strong enough in waters where they would dissolve. Weak calcification may result during the ecdysis (moulting) of the ostracods carapace (Keyser and Walter, 2004). Consequently, ostracods that inhabit waters with low calcium concentration or high salinity may not fossilize well (e.g., not enough time for calcification, strong acidity, moulting stage, etc.).
Unlike Ht. salina, little ecological information is available for He. intermedia found only once in a trough during this study. The species is known from several different types of 14 aquatic habitats (e.g., creek, spring, stream, pond, pool, littoral zones of lake and reservoir) (see details in Külköylüoǧlu et al., 2012d; Akdemir and Külköylüoǧlu, 2014; Uçak et al., 2014; Yavuzatmaca et al., 2015). Water temperatures in these environments ranged from 13.9 to 32.3 °C, Ca (8.09–119.13 ppm), and Mg (5.54–48.20 ppm). Two earlier studies (Wansard et al., 1999; Wansard and Mezquita, 2001) specifically focused on the correlation between water and carapace chemistry of this species. Wansard et al. (1999) collected He. intermedia from the River Magre (Valencia, Spain) with a broad water temperature range (5–20 °C) and with conductivity values less than 1 mS/cm, and the ratio of Mg/Ca of the water measured between 0.1 and 1. Wansard et al. (1999) reported that temperature was not an influential factor in the partition coefficient value of Mg (D(Mg)). During the present study, we measured water Ca and Mg levels as 51.54 and 20.41 ppm, respectively. The ratio of Mg/Ca of the water was about 0.396 ppm, similar to that of earlier studies. Besides, Wansard and Mezquita (2001) indicated that temperature was not an influential factor in the elements of the carapace. However, the opposite results calculated from their data were also found (see details in Dettman et al., 2002). The implication of these results suggest that He. intermedia prefer slightly acidic (pH 6–6.04) (Külköylüoǧlu et al., 2012d; Yavuzatmaca et al., 2015) to alkaline freshwater habitats (pH 7.2–8.5) (Wansard and Mezquita, 2001). Increasing salinity may decrease in the ratios of Sr/Ca and Mg/Ca (Wansard and Mezquita, 2001). Thereby, Ca is a dominant element in He. intermedia carapace that may explain its common occurrences in alkaline spring waters. Chivas et al. (1985) argued that Sr in the valves of all ostracods, within the same genus, is not affected by water temperature; therefore, Sr values in carapace may correspond to the Sr in waters. Except for two genera 15 (Potamocypris and Heterocypris), species of other genera did not support the view of Chivas et al. (1985).
4.3 Effectiveness of EDX in detecting heavy metal on the carapace surface
Anthropogenic impacts, especially industrial activities, create an intense disturbance on aquatic ecosystems (Alin et al., 1999). One of the most important factors that cause this pollution is heavy metals. On the other hand, abundance and diversity of the ostracods can be affected by the metals in their surrounding water (Ruiz et al., 2013). However, it has also been observed that some ostracod species are quite resistant to metal pollution such as lead (Prasuna et al., 1996). Although it gives different results to different types of pollution, it is known that the diversity of ostracods is inversely proportional to pollution (Ruiz et al., 2005). In short, it is one of the responsibilities of hydrobiologists to analyze both the amount of metal contamination of the aquatic habitat and whether the organism uptakes the metal.
The method tested in the present study is to apply EDX analysis by focusing the center of the carapace during SEM monitoring. The data displays the atomic and molar percentages of elements that belonging to the shell surface in a frame. Elements such as carbon, oxygen, calcium, magnesium are not useful since they do not give what compound they belong to. On the other hand, it only scans limited part of the surface and it is insufficient to generate a full range of carapace chemistry data. Since EDX scanning of samples prepared for SEM monitoring does not require any extra preparation or processing, it is thought that it can be functional in obtaining a quick preliminary idea about the presence of trace elements like heavy metals. In this regard, the heavy metals found in some of the 17 different sample scans made suggested that the method could yield efficient results when used for this purpose. Likewise, heavy metals do not give a clear result because there is only one sample belonging to the same habitat in the present study. In a hypothetical study where heavy metal traces were found consistently in a study with EDX analysis results with all SEM monitoring, it could provide evidence of heavy metal pollution in the studied habitat.
5 Conclusion
The species distribution observed in the field shows a high tolerance and optimum values for salinity and temperature. For example, Ht. salina and I. bradyi are widely spread over the region among a variety of habitats. An exception was P. olivaceus. While occurring in seven different habitat types (stream, river, creek, trough, waterfall, water body, and pool) along with the mountain ranges, P. olivaceus remains limited in the northern part of the Giresun province in good agreement with the species' negative correlation to altitude (Külköylüoǧlu et al., 2013). Still, some other factors (e.g., biotic factors, not discussed herein due to lack of biological data) can also affect its distribution. Similarly, I. inermis and Po. fulva wer found within the Dereli region (Fig. 1). Psychrodromus olivaceus thrives mainly in cold running waters and/or springs, spring-related streams, lakes, caves, and rice fields (Baltanás et al., 1993; Meisch 2000). In some cases (e.g., this study), the species exists in troughs. Comparative analyses between chemical contents of sampling sites located on southern and northern regions of the Giresun province revealed two factors (elevation and water temperature) were statistically significant differences. At the same time, pH, EC, and DO were not significant (P > 0.05). Since water temperature tends to decrease with increasing elevation, interpretation of these results appears to provide supportive evidence that these factors are highly influential on the distribution of P. olivaceus. Similar ideas would also be used to apply for other species (e.g., Po. fulva) if there were enough amounts of ecological data available.
Declaration of competing interest
The authors declare no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Supplementary Material
Figure S1. SEM photographs of some ostracods in this study.
Table S1. Effective factors on the ostracod species determined by the present and previous studies.
Table S2. Numbers of stations and species found during this study from different habitat types in Giresun province.
Access hereAcknowledgments
We thank to Dr. Manuel R. Palacios-Fest (Terra Nostra Earth Sciences Research, LLC, Arizona, USA) for his review and suggestions on the manuscript. Also, Drs. Necati Karakaya and Muazzez Çelik-Karakaya (Konya Technique University) are thanked for information about water quality measurements in their studies. Dr. Nusret Karakaya (Bolu Abant İzzet Baysal University) is also appreciated for his help during major ion analyses. We also thank our graduate students (Filiz Batmaz, Enes Dalgakıran, Ozan Yılmaz, Umutcan Gürer, Enis Akay) for their continuous assistance during the field and laboratory work. Also, we recognize Emine Demirtürk Yerebasmaz (Bolu Abant İzzet Baysal University) for her assistance during SEM photography. This study was supported by the TÜBİTAK, Project No: 2130172.
References
- Akdemir D. 2008. Differences in Ostracoda (Crustacea) assemblages between two Maar Lakes and one Sinkhole Lake in the Konya region of Turkey. Turk J Zool 32: 107–113. [Google Scholar]
- Akdemir D, Külköylüoǧlu O. 2014. Preliminary study on distribution, diversity, and ecological characteristics of nonmarine Ostracoda (Crustacea) from the Erzincan region (Turkey). Turk J Zool 38: 421–431. [CrossRef] [Google Scholar]
- Akdemir D, Külköylüoǧlu O, Yavuzatmaca M, Sarı N. 2016. Freshwater ostracods (Crustacea) of Gaziantep (Turkey) and their habitat preferences according to movement ability. Fundam Appl Limnol 187: 307–314. [CrossRef] [Google Scholar]
- Alin SR, Cohen AS, Bills R, et al. 1999. Effects of landscape disturbance on animal communities in Lake Tanganyika, East Africa. Conserv Biolo 13: 1017–1033. [CrossRef] [Google Scholar]
- Balian E, Harrison IJ, Barber-James H, et al. 2010. A wealth of life: Species diversity in freshwater systems. In: Freshwater: The Essence of Life, edited by R.A. Mittermeier, T.A. Farrell, I.J. Harrison, A.J. Upgren, T.M. Brooks. CEMEX Publication, 50–89. [Google Scholar]
- Baltanás A, Danielopol DL, Rosell JR, Marmonier P. 1993. Psychrodromus betharrami n.sp. (Crustacea, Ostracoda): morphology, ecology, and biogeography. Zool Anz 231: 39–57. [Google Scholar]
- Benson RH. 1990. Ostracoda and the discovery of global Cainozoic palaeoceanographical events. In: Ostracoda and Global events, edited by R. Whatley, C. Maybury, 41–59. [Google Scholar]
- Birks HJB, Line JM, Juggins S, Stevenson AC, ter Braak CJF. 1990. Diatoms and pH reconstruction. Philos Trans R Soc London B 327: 263–278. [CrossRef] [Google Scholar]
- Bottazzi E, Bruno MC, Pieri V, et al. 2011. Spatial and seasonal distribution of invertebrates in Northern Apennine rheocrene springs. J Limnol 70: 77–92. [CrossRef] [Google Scholar]
- Bunbury J, Gajewski K. 2005. Quantitative analysis of freshwater ostracode assemblages in southwestern Yukon Territory, Canada. Hydrobiologia 545: 117–128. [CrossRef] [Google Scholar]
- Chivas AR, De Deckker P, Shelley JMG. 1985. Strontium content of ostracods indicates lacustrine palaeosalinity. Nature 316: 251–253. [CrossRef] [Google Scholar]
- Chivas AR, De Deckker P, Shelley JMG. 1986. Magnesium content of nonmarine ostracod shells: a new palaeosalinometer and palaeothermometer. Palaeogeogr Palaeoclimatol Palaeoecol 54: 43–61. [CrossRef] [Google Scholar]
- Cohen CA, Morin JG. 1990. Patterns of reproduction in ostracodes: a review. J Crust Biol 10: 184–211. [CrossRef] [Google Scholar]
- Coviaga C, Cusminsky G, Pérez P. 2018. Ecology of freshwater ostracods from Northern Patagonia and their potential application in paleoenvironmental reconstructions. Hydrobiologia 816: 3–20. [CrossRef] [Google Scholar]
- Danielopol LD, Marmonier P, Boulton AJ, Bonaduce G. 1994. World subterranean ostracod biogeography: dispersal or vicariance. Hydrobiologia 287: 119–129. [CrossRef] [Google Scholar]
- Delorme LD. 1991. Ostracoda. In: Ecology and Classification of North American Invertebrates, edited by J.H. Thorpe and A.P. Covich. New York: Academic Press, pp. 811–850. [Google Scholar]
- Dettman DL, Palacios-Fest M, Cohen AS. 2002. Comment on G. Wansard & F. Mezquita, the response of ostracode shell chemistry to seasonal change in a Mediterranean freshwater spring environment. J Paleolimnol 27: 487–491. [CrossRef] [Google Scholar]
- Dole-Olivier M-J, Galassi D, Marmonier P, Creuzé des Chatelliers M. 2001. The biology and ecology of lotic microcrustaceans. Freshw Biol 44: 63–91. [Google Scholar]
- Dügel M, Külköylüoǧlu O, Kılıç M. 2008. Species assemblages and habitat preferences of Ostracoda (Crustacea) in Lake Abant (Bolu, Turkey). Belgian J Zool 138: 50–59. [Google Scholar]
- Escrivà A, Poquet J, Mesquita-Joanes F. 2015. Effects of environmental and spatial variables on lotic ostracod metacommunity structure in the Iberian Peninsula. Intl Waters 5: 283–294. [Google Scholar]
- Escrivà A, Rueda J, Armengol X, Mesquita-Joanes F. 2014. Artificial dam lakes as suitable habitats for exotic invertebrates: Ostracoda ecology and distribution in reservoirs of the Eastern Iberian Peninsula. Knowl Manag Aquat Ecosyst 412: 1–12. [Google Scholar]
- Fuhrmann R. 2013. Atlas Quartärer und Rezenter Ostrakoden Mitteldeutschlands, Mauritiana, 320 p. [Google Scholar]
- Gandolfi A, Todeschi EBA, Van Doninck K, Rossi V, Menozzi P. 2001. Salinity tolerance of Darwinula stevensoni (Crustacea, Ostracoda), Ital J Zool 68: 61–67. [CrossRef] [Google Scholar]
- Guo Y, Frenzel P, Börner N, Akıta LG, Zhu L. 2013. Recent Ostracoda of Taro Co (Western Tibetan Plateau). Nat Sicil 37: 161–162. [Google Scholar]
- Gürer U, Külköylüoğlu O. 2019. Limnoecological characteristics and seasonal distribution of Ostracoda (Crustacea) in a natural lake (Lake Karagöl) and a man-made reservoir (Lake Uşak) in northeastern Turkey. Bull Soc Nat luxemb 121: 277–289. [Google Scholar]
- Horne DJ Baltanás A, Paris G. 1998. Geographical distribution of reproductive modes in living nonmarine ostracodes. In: Sex and parthenogenesis: evolutionary ecology of reproductive modes in nonmarine ostracods, edited by K. Martens. Leiden, Netherlands: Backhuys Publishers, pp. 77– 99. [Google Scholar]
- Horne DJ, Boomer I. 2000. The role of Ostracoda in saltmarsh meiofaunal communities. In: British Saltmarshes, Forrest Text, Cardigan, for the Linnean Society of London, edited by B.R. Sherwood, B.G. Gardiner, T. Harris, pp. 182– 202. [Google Scholar]
- Horne F. 1993. Survival strategy to escape desiccation in a freshwater ostracod. Crustaceana 65: 53–61. [CrossRef] [Google Scholar]
- Iglikowska A, Namiotko T. 2012. The impact of environmental factors on diversity of Ostracoda in freshwater habitats of subarctic and temperate Europe. Ann Zool Fennici 49: 193–218. [CrossRef] [Google Scholar]
- Ito E, De Deckker P, Eggins S. 2003. Ostracodes and their shell chemistry: Implications for paleohydrologic and paleoclimatologic applications. Paleontol Soc Pap 9: 119–152. [CrossRef] [Google Scholar]
- Juggins S. 2003. Software for ecological and palaeoecological data analysis and visualization − C2 User Guide, University of Newcastle, Newcastle-upon-Tyne, UK, 69 p. [Google Scholar]
- Karakaya N, Çelik Karakaya M. 2014. Toxic element contamination in waters from the massive sulfide deposits and wastes around Giresun, Turkey. Turk J Earth Sci 23: 113–128. [CrossRef] [Google Scholar]
- Karakaya N, Karakaya MÇ, Nalbantçılar MT, Yavuz F. 2007. Relation between spring water chemistry and hydrothermal alteration in the Şaplıca volcanic rocks, Şebinkarahisar (Giresun, Turkey). J Geochemical Explor 93: 35–46. [CrossRef] [Google Scholar]
- Karanovic I. 2012. Recent freshwater ostracods of the world, Springer-Verlag Berlin Heidelberg, 608 p. [Google Scholar]
- Keyser D, Walter R. 2004. Calcification in ostracodes. Rev Española Micropaleontol 36: 1–11. [Google Scholar]
- Khangarot BS, Das S. 2009. Acute toxicity of metals and reference toxicants to a freshwater ostracod, Cypris subglobosa Sowerby, 1840 and correlation to EC50 values of other test models. J Hazard Mater 172: 641–649. [CrossRef] [PubMed] [Google Scholar]
- Kılıç M. 2001. Recent Ostracoda (Crustacea) fauna of the Black Sea coasts of Turkey. Turk J Zool 25: 375–388. [Google Scholar]
- Külköylüoğlu O. 1998. Freshwater Ostracoda and their quarterly occurrence in Şamlar Lake (İstanbul, Turkey). Limnologica 28: 229–235. [Google Scholar]
- Külköylüoğlu O. 1999. Seasonal distribution of freshwater Ostracoda (Crustacea) in springs of Nevada. Geosound 35: 85–91. [Google Scholar]
- Külköylüoğlu O. 2003. Ecology of freshwater Ostracoda (Crustacea) from lakes and reservoirs in Bolu, Turkey. J Freshw Ecol 18: 343–347. [Google Scholar]
- Külköylüoǧlu O. 2005a. Factors affecting the occurrence of Ostracoda (Crustacea) in the Yumrukaya Reedbeds (Bolu, Turkey). Wetlands 25: 224–227. [CrossRef] [Google Scholar]
- Külköylüoğlu O. 2005b. Ecology and phenology of freshwater ostracods in Lake Gölköy (Bolu, Turkey). Aquat Ecol 39: 295–304. [Google Scholar]
- Külköylüoğlu O. 2013. Diversity, distribution, and ecology of nonmarine Ostracoda (Crustacea) in Turkey: application of pseudorichness and cosmoecious species concepts. Transw Res Netw India Recent Res Devel Ecol 4: 1–18. [Google Scholar]
- Külköylüoǧlu O, Akdemir D, Sarı N, Yavuzatmaca M, Oral C, Başak E. 2013. Distribution and ecology of Ostracoda (Crustacea) from troughs in Turkey. Turk J Zool 37: 277–287. [Google Scholar]
- Külköylüoǧlu O, Dügel M. 2004. Ecology and spatiotemporal patterns of Ostracoda (Crustacea) from Lake Gölcük (Bolu, Turkey). Arch Hydrobiol 160: 67–83. [CrossRef] [Google Scholar]
- Külköylüoǧlu O, Dügel M, Kılıç M. 2007. Ecological requirements of Ostracoda (Crustacea) in a heavily polluted shallow lake, Lake Yeniçağa (Bolu, Turkey). Hydrobiologia 585: 119–133. [CrossRef] [Google Scholar]
- Külköylüoğlu O, Palacios-Fest MR, Baron D, Sarı N. 2015. Monthly variations in the shell structure of two freshwater ostracod (Crustacea) species in Karapınar Spring (Bolu, Turkey). Turk J Zool 39: 906–916. [CrossRef] [Google Scholar]
- Külköylüoǧlu O, Sarı N. 2012. Ecological characteristics of the freshwater Ostracoda in Bolu Region (Turkey). Hydrobiologia 688: 37–46. [CrossRef] [Google Scholar]
- Külköylüoǧlu O, Akdemir D, Yüce R. 2012a. Distribution, ecological tolerance, and optimum levels of freshwater Ostracoda (Crustacea) from Diyarbakır, Turkey. Limnology 13: 73–80. [CrossRef] [Google Scholar]
- Külköylüoǧlu O, Sarı N, Akdemir D. 2012b. Distribution and ecological requirements of ostracods (Crustacea) at high altitudinal ranges in Northeastern Van (Turkey). Ann Limnol 48: 39–51. [CrossRef] [EDP Sciences] [Google Scholar]
- Külköylüoǧlu O, Sarı N, Akdemir D, Yavuzatmaca M, Altınbaǧ C. 2012c. Distribution of sexual and asexual Ostracoda (Crustacea) from different altitudinal ranges in the Ordu region of Turkey: Testing the Rapoport rule. High Alt Med Biol 13: 126–137. [CrossRef] [PubMed] [Google Scholar]
- Külköylüoǧlu O, Yavuzatmaca M, Akdemir D, Sarı N. 2012d. Distribution and local species diversity of freshwater Ostracoda in relation to habitat in the Kahramanmaraş Province of Turkey. Int Rev Hydrobiol 97: 247–261. [CrossRef] [Google Scholar]
- Külköylüoǧlu O, Sarı N, Dügel M, Dere Ş, Dalkıran N, Aygen C, et al. 2014. Effects of limnoecological changes on the Ostracoda (Crustacea) community in a shallow lake (Lake Çubuk, Turkey). Limnologica 46: 99–108. [CrossRef] [Google Scholar]
- Külköylüoğlu O, Yavuzatmaca M, Akdemir D, Çelen E, Dalkıran N. 2018. Ecological classification of the freshwater Ostracoda (Crustacea) based on physicochemical properties of waters and habitat preferences. Ann Limnol- Int J Lim 54: 26–37. [CrossRef] [EDP Sciences] [Google Scholar]
- Külköylüoğlu O, Yavuzatmaca M, Akdemir D, Yılmaz O, Çelen E, Dere Ş, et al. 2019a. Correlational patterns of species diversity, swimming ability, and ecological tolerance of nonmarine Ostracoda (Crustacea) with different reproductive modes in shallow water bodies of ağrı region (Turkey). J Freshw Ecol 34: 151–165. [CrossRef] [Google Scholar]
- Külköylüoğlu O, Akdemir D, Yavuzatmaca M, Çelen E, Dere Ş, Dalkıran N. 2019b. Do reproductive modes and swimming ability influence occurrence of nonmarine ostracod (Crustacea) species among aquatic habitats? Zool Sci 36: 511–520. [CrossRef] [PubMed] [Google Scholar]
- Külköylüoğlu O, Yavuzatmaca M, Sarı N, Akdemir D. 2016. Elevational distribution and species diversity of freshwater Ostracoda (Crustacea) in Çankırı region (Turkey). J Freshw Ecol 31: 219–230. [CrossRef] [Google Scholar]
- Külköylüoğlu O, Yavuzatmaca M, Yılmaz O. 2020. Ecology and distribution of ostracods in Mardin and Muş provinces in Turkey. Biologia 75: 1855–1870. [CrossRef] [Google Scholar]
- Külköylüoǧlu O, Yılmaz S, Yavuzatmaca M. 2017. Comparison of Ostracoda (Crustacea) species diversity, distribution, and ecological characteristics among habitat types. Fundam Appl Limnol 190: 63–86. [CrossRef] [Google Scholar]
- Laprida C, Díaz A, Ratto N. 2006. Ostracods (Crustacea) from thermal waters, southern Altiplano, Argentina. Micropaleontology 52: 177–188. [CrossRef] [Google Scholar]
- Lerner-Seggev R. 1968. The fauna of Ostracoda in Lake Tiberias. Israel J Zool 17: 117–143. [Google Scholar]
- Li X, Liu W, Zhang L, Sun Z. 2010. Distribution of Recent ostracod species in the Lake Qinghai area in northwestern China and its ecological significance. Ecol Indic 10: 880–890. [CrossRef] [Google Scholar]
- Martínez-García B, Suarez-Hernando O, Mendicoa J, Murelaga X. 2015. Living ostracod species from permanent and semi-permanent ponds of Bardenas Reales de Navarra (Northern Spain) with remarks on their ecological requirements. Ameghiniana 52: 598–612. [CrossRef] [Google Scholar]
- Martins MJF, Namiotko T, Cabral MC, Fatela F, Boavida MJ. 2010. Contribution to the knowledge of freshwater Ostracoda fauna in continental Portugal, with an updated checklist of Recent and Quaternary species. J Limnol 69: 160–173. [CrossRef] [Google Scholar]
- Meisch C. 2000 Freshwater Ostracoda of Western and Central Europe, Heidelberg: Spektrum Akademischer Verlag, Süßwasserfauna von Mitteleuropa, 522 p. [Google Scholar]
- Meisch C, Broodbakker NW. 1993. Freshwater Ostracoda (Crustacea) collected by prof. J. H. Stock on the Canary and Cape Verde islands. With an annotated checklist of the freshwater Ostracoda of the Azores, Madeira, the Canary, the Selvagens, and Cape Verde islands. Trav sci Mus nat hist nat Luxemb 19: 3–47. [Google Scholar]
- Meisch C, Mary-Sasal N, Colin J, Wouters K. 2007. Freshwater Ostracoda (Crustacea) collected from the islands of Futuna and Wallis, Pacific Ocean, with a checklist of the nonmarine Ostracoda of the Pacific Islands. Bull la Société des Nat Luxemb 108: 89–103. [Google Scholar]
- Meisch C, Smith RJ, Martens K. 2019. A subjective global checklist of the extant nonmarine Ostracoda (Crustacea). Eur J Taxon 1–135. [Google Scholar]
- Meteorological Service of Republic of Turkey. 2019. https://mgm.gov.tr/Giresun [Google Scholar]
- Mezquita F, Griffiths HI, Domínguez MI, Lazano-Quilis MA. 2001. Ostracoda (Crustacea) as ecological indicators: a case study from Iberian Mediterranean brooks. Archiv für Hydrobiolog 150: 545–560. [CrossRef] [Google Scholar]
- Mezquita F, Hernández R, Rueda J, 1999. Ecology and distribution of ostracods in a polluted Mediterranean river. Palaeogeogr Palaeoclimatol Palaeoecol 148: 87–103. [CrossRef] [Google Scholar]
- Mischke S, Almogi-Labin A, Ortal R, Rosenfeld A, Schwab MJ, Boomer I. 2010. Quantitative reconstruction of lake conductivity in the Quaternary of the Near East (Israel) using ostracods. J Paleolimnol 43: 667–688. [CrossRef] [Google Scholar]
- Nagorskaya L, Keyser D. 2005. Habitat diversity and ostracod distribution patterns in Belarus. Hydrobiologia 538: 167–178. [Google Scholar]
- Nazik A, Groos-Uffenorde H, Olempska E, Yalçın MN, Wilde V, Schindler E, et al. 2018. Late Silurian and Devonian ostracods of the Istanbul Zone (Western Pontides) and the Taurides: palaeogeographical implications. Palaeobio Palaeoenv 98: 593–612. [CrossRef] [Google Scholar]
- Palacios-Fest MR, Cohen AS, Anadón P. 1994. Use of ostracodes as paleoenvironmental tools in the interpretation of ancient lacustrine records. Rev Esp Paleontol 9: 145–162. [Google Scholar]
- Pax F. 1942. Die Crustaceen der deutschen Mineralquellen. Der naturforschenden Gesellschaft zu Görlitz 33: 87–130. [Google Scholar]
- Pax F. 1948. Die Tierwelt der mitteleuropäischen Schwefelquellen. Senckenbergiana 28: 139–152. [Google Scholar]
- Pérez L, Lorenschat J, Brenner M, Scharf B, Schwalb A. 2010. Extant freshwater ostracodes (Crustacea: Ostracoda) from Lago Petén itzá, Guatemala. Rev Biol Trop 58: 871–895. [PubMed] [Google Scholar]
- Peterson DE, Finger KL, Iepure S, Mariani S, Montanari A, Namiotko T. 2013. Ostracod assemblages in the frasassi caves and adjacent sulfidic spring and sentino river in the northeastern of Italy. J Cave Karst Stud 75: 11–27. [CrossRef] [Google Scholar]
- Pieri V, Martens K, Stoch F, Rossetti G. 2009. Distribution and ecology of non-marine ostracods (Crustacea, Ostracoda) from Friuli Venezia Giulia (NE Italy). J Limnol 68: 1–15. [CrossRef] [Google Scholar]
- Pint A, Frenzel P, Horne DJ, Franke J, Daniel T, Burghardt A, et al. 2015. Ostracoda from inland water bodies with saline influence in Central Germany: Implications for palaeoenvironmental reconstruction. Palaeogeogr Palaeoclimatol Palaeoecol 419: 37–46. [CrossRef] [Google Scholar]
- Prasuna G, Zeba M, Khan MA, 1996. Excretion of lead as a mechanism for survival in Chrissia halyi (Ferguson, 1969). Bull Environ Contam Toxicol 57: 849–852. [CrossRef] [PubMed] [Google Scholar]
- Rieradevall M, Roca JR. 1995. Distribution and population dynamics of ostracodes (Crustacea, Ostracoda) in a karstic lake: Lake Banyoles (Catalonia, Spain). Hydrobiologia 310: 189–196. [CrossRef] [Google Scholar]
- Rosati M, Cantonati M, Primicerio R, Rossetti G. 2014. Biogeography and relevant ecological drivers in spring habitats: A review on ostracods of the western Palearctic. Int Rev Hydrobiol. 99: 409–424. [CrossRef] [Google Scholar]
- Rossi V, Benassi G, Veneri M, Bellavere C, Menozzi P, Moroni A, et al. 2003. Ostracoda of the Italian ricefields thirty years on: new synthesis and hypothesis. J Limnol. 62: 1–8. [CrossRef] [Google Scholar]
- Ruiz F, Abad M, Bodergat AM, Carbonel P, Rodríguez-Lázaro J, González-Regalado ML, et al. 2013. Freshwater ostracods as environmental tracers. Int J Environ Sci Technol 10: 1115–1128. [CrossRef] [Google Scholar]
- Ruiz F, Abad M, Bodergat AM, Carbonel P, Rodríguez-Lázaro J, Yasuhara M. 2005. Marine and brackish-water ostracods as sentinels of anthropogenic impacts. Earth-Sci Rev 72: 89–111. [CrossRef] [Google Scholar]
- Ruiz F, González-Regalado ML, Borrego J, Abad M, Pendón JG. 2004. Ostracoda and foraminifera as short-term tracers of environmental changes in very polluted areas: The Odiel Estuary (SW Spain). Environ Pollut 129: 49–61. [CrossRef] [PubMed] [Google Scholar]
- Scharf B, Herzog M, Pint A. 2016. New occurrences of Cyprideis torosa (Crustacea, Ostracoda) in Germany. J Micropalaeontol 36: 120–126. [Google Scholar]
- Shuhaimi-Othman M, Yakub N, Ramle NA, Abas A. 2011. Toxicity of metals to a freshwater ostracod: Stenocypris major. J Toxicol 1–8. [CrossRef] [Google Scholar]
- Smith AJ, Horne DJ. 2002. Ecology of marine, marginal marine and nonmarine Ostracodes. In: The Ostracoda: Applications in Quaternary Research, Geophysical Monograph, edited by J.A. Holmes and A.R. Chivas. pp. 37–64. [Google Scholar]
- Szlauer-Łukaszewska A. 2014. The dynamics of seasonal ostracod density in groyne fields of the Oder River (Poland). J Limnol 73: 96–109. [Google Scholar]
- ter Braak CJF. 1987. The analysis of vegetation-environment relationships by canonical correspondence analysis. Vegetatio 69: 69–77. [CrossRef] [Google Scholar]
- Torres-Saldarriaga A, Martínez JI. 2010. Ecology of non-marine Ostracoda from La Fe Reservoir (El Retiro, Antioquia) and their potential application in paleoenvironmental studies. Rev Acad Colomb Cienc Exactas Fis Nat 34: 397–409. [Google Scholar]
- Tuncer A, Tunoğlu C. 2015. Early Pleistocene (Calabrian) Ostracoda assemblage and paleoenvironmental characteristics of the Fevzipaşa Formation, Western Anatolia. Micropaleontology 61: 69–83. [CrossRef] [Google Scholar]
- Tunoğlu C. 2003. Systematics and biostratigraphy of the Pontian Candoninae (Ostracoda) from the Eastern Black Sea Region (Northern Turkey). Geolog Carpathica 54: 21–40. [Google Scholar]
- Turpen JB, Angel RW, 1971. Aspects of molting and calcification in the ostracod Heterocypris. Biol Bull 140: 331–338. [CrossRef] [Google Scholar]
- Uçak S, Külköylüoğlu O, Akdemir D, Başak E. 2014. Distribution, diversity, and ecological characteristics of freshwater Ostracoda (crustacea) in shallow aquatic bodies of the Ankara region, Turkey. Wetlands 34: 309–324. [CrossRef] [Google Scholar]
- Valls L, Rueda J, Mesquita-Joanes F. 2014. Rice fields as facilitators of freshwater invasions in protected wetlands: The case of Ostracoda (Crustacea) in the Albufera Natural Park (E Spain). Zool Stud 53: 1–10. [CrossRef] [Google Scholar]
- Valls L, Castillo-Escrivà A, Mesquita-Joanes F, Armengol X. 2016. Human-mediated dispersal of aquatic invertebrates with waterproof footwear. Ambio 45: 99–109. [CrossRef] [PubMed] [Google Scholar]
- van der Meeren T, Almendinger JE, Ito E, Martens K. 2010. The ecology of ostracodes (Ostracoda, Crustacea) in western Mongolia. Hydrobiologia 641: 253–273. [CrossRef] [Google Scholar]
- Van Doninck K, Schön I, Martens K, Goddeeris B. 2003. The life-cycle of the asexual ostracod Darwinula stevensoni (Brady & Robertson, 1870) (Crustacea, Ostracoda) in a temporate pond. Hydrobiologia 500: 331–340. [CrossRef] [Google Scholar]
- van Harten D. 1983. Resource competition as a possible cause of sex ratio in benthic Ostracodes. In: Applications of Ostracoda, edited by R.F. Maddocks. Houston: Univ. Houston Geosciences, 568–580. [Google Scholar]
- Viehberg FA. 2006. Freshwater ostracod assemblages and their relationship to environmental variables in waters from northeast Germany. Hydrobiologia 571: 213–224. [CrossRef] [Google Scholar]
- Wansard G, Mezquita F. 2001. The response of ostracod shell chemistry to seasonal change in a Mediterranean freshwater spring environment. J Paleolimnol 25: 9–16. [CrossRef] [Google Scholar]
- Wansard G, Roca JR, Mezquita F, 1999. Experimental determination of strontium and magnesium partitioning in calcite of the freshwater ostracod Herpetocypris intermedia. Arch Hydrobiol 145: 237–253. [CrossRef] [Google Scholar]
- Williams M, Siveter D, Salas M, Vannier J, Popov LE, Ghobadi-Pour M. 2008. The earliest ostracods: the geological evidence. Senck leth 88: 11–21. [CrossRef] [Google Scholar]
- Wise CD. 1961. Taxonomy and ecology of freshwater ostracods of south-Central Texas. PhD, University of New Mexico, Las Cruces, USA. [Google Scholar]
- Yavuzatmaca M. 2019. Comparative analyses of nonmarine ostracods (Crustacea) among water basins in Turkey. Acta Zool Acad Sci Hungaricae 65: 269–297. [CrossRef] [Google Scholar]
- Yavuzatmaca M, Külköylüoğlu O, Yılmaz O. 2015. Distributional patterns of non-marine Ostracoda (Crustacea) in Adıyaman province (Turkey). Ann Limnol 51: 101–113. [CrossRef] [EDP Sciences] [Google Scholar]
- Yavuzatmaca M, Külköylüoǧlu O. 2019. Reporting of sexual population of Heterocypris incongruens (Ramdohr, 1808) from a man-made pond (Kahramanmaraş, Turkey) and comparison of hemipenes of the genus Heterocypris (Claus, 1892). Acta Aquat Turc 15: 139–150. [CrossRef] [Google Scholar]
- Yavuzatmaca M, Külköylüoğlu O, Akdemir D, Çelen E. 2018. On the relationship between the occurrence of ostracod species and elevation in Sakarya province, Turkey. Acta Zool Acad Sci Hungaricae 64: 329–354. [CrossRef] [Google Scholar]
- Yavuzatmaca M, Külköylüoğlu O, Yılmaz O. 2017a. Estimating distributional patterns of nonmarine Ostracoda (Crustacea) and habitat suitability in the Burdur province (Turkey). Limnologica 62: 19–33. [CrossRef] [Google Scholar]
- Yavuzatmaca M, Külköylüoğlu O, Yılmaz O, Akdemir D. 2017b. On the Relationship of Ostracod Species (Crustacea) to Shallow Water Ion and Sediment Phosphate Concentration Across Different Elevational Range (Sinop, Turkey). Turkish J Fish Aquat Sci 17: 1333–1346. [Google Scholar]
- Yılmaz F, Külköylüoğlu O. 2006. Tolerance, optimum ranges, and ecological requirements of freshwater Ostracoda (Crustacea) in Lake Aladaǧ (Bolu, Turkey). Ecol Res 21: 165–173. [CrossRef] [Google Scholar]
Cite this article as: Çapraz Ç, Külköylüoğlu O, Akdemir D, Yavuzatmaca M. 2022. Determining effective environmental factors and ecology of non-marine Ostracoda (crustacea) in Giresun, Turkey. Int. J. Lim. 58: 3:
All Tables
Comparison of the habitat types in the Giresun province with collected ostracods.
CCA summary table with four variables (electrical conductivity, magnesium, nitrate and water temperature) and nine species with three or more times occurrences from the Giresun province (*DCA results).
Tolerance (Tol) and optimum (Opt) values for the nine most common species against the variables measured from each sampling site. Abbreviations: Count (numbers of species occurrence), Max (maximum numbers of individuals), N2 (Hill's coefficient or measure of effective number of occurrences), dissolved oxygen (DO, mg l−1), electrical conductivity (EC, μS cm−1), water temperature (Tw, °C), redox potential (ORP), elevation (Elev), sodium (Na2+, ppm) in water, magnesium (Mg2+, ppm) in water, calcium (Ca2+, ppm) in water, fluoride (F–, ppm) in water, chloride (Cl–, ppm) in water, total phosphate (T.PO4 3–, ppm) in sediment.
Elemental atomic percentage (%) values from the carapace surface of 17 ostracod species according to EDX analyses. Elements found in trace amounts are listed under ‘Others’. Numbers written in parentheses indicate the number of sampling site.
A) Mean, minimum (Min) and maximum (Max) values of environmental, and B) chemical variables measured from the sampling sites. Abbreviations: DO, dissolved oxygen; EC (electrical conductivity); Tw (water temperature); Atmp (atmospheric pressure); ORP (oxidation-reduction potential); elevation (Elev); Sal (salinity); TDS (total dissolved solids); sodium (Na2+); chloride (Cl–); magnesium (Mg2+); calcium (Ca2+); nitrite (NO2 –); nitrate (NO3 –); sulphate (SO4 2 –); total phosphate T.PO4 3 –. (*) eight meters below the sea level. Ion values are in ppm.
All Figures
Fig. 1 Total of 105 randomly selected sampling sites (numbers shown on the map from 1 to 105) from 16 counties (Merkez, Alucra, Bulancak, Çamoluk, Çanakçı, Dereli, Doğakent, Espiye, Eynesil, Görele, Güce, Keşap, Piraziz, Şebinkarahisar, Tirebolu, Yağlıdere) of the Giresun province, Turkey. |
|
In the text |
Fig. 2 The CCA diagram indicates the relationship between four ecological variables (water temperature (Tw), the magnesium content of water (Mg), elevation (Elev), electrical conductivity (EC)) and nine species (Neglecandona neglecta (NN), Ht. incongruens (HI), Ht. salina (HSa), I. bradyi (IBr), Po. fallax (PF), Po. fulva (PFu), Psychrodromus olivaceus (PO), P. fontinalis (PFo), Po. villosa (PVi)) from 64 different sampling sites in the Giresun province. |
|
In the text |
Fig. 3 Distribution of ostracod species (Psychrodromus olivaceus, Potamocypris fulva) in the Giresun province. Empty sites simply “absence of ostracods”. |
|
In the text |
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