Turk J Zool 34 (2010) 225-230 © TÜBİTAK Research Article doi:10.3906/zoo-0902-25

Ostracods (Crustacea) and habitat similarities in the region ()

Necmettin SARI, Okan KÜLKÖYLÜOĞLU* Abant İzzet Baysal University, Faculty of Arts and Science, Department of Biology, Gölköy TR-14280, Bolu - TURKEY

Received: 25.02.2009

Abstract: A total of 41 freshwater ostracod species belonging to 21 genera was collected from 144 different aquatic bodies in the Bolu region during the summer of 2006. The genus Schellencandona and 12 species (Candona weltneri, C. sanociensis, C. lactea, Fabaeformiscandona cf. breuili, F. balatonica, F. brevicornis, F. protzi, F. latens, Schellencandona cf. belgica, Pseudocandona cf. semicognita, Potamocypris similis, and P. smaragdina) are new for the Turkish Ostracoda fauna. Additionally, 5 other species (Herpetocypris brevicaudata, Heterocypris salina, H. rotundata, Cyclocypris laevis, Trajancypris serrata) are new for Bolu. UPGMA analyses showed districts of Bolu in 5 clustering groups. The highest habitat similarity (75%) was found between Yeniçağa and Göynük, while the least (20%) was observed between and Merkez districts. Shannon-Weaver diversity suggested the highest evenness for ostracods at Dörtdivan (0.95) and the highest diversity index (H’) at Merkez district (2.63). Mechanisms of species dispersion are numerous, and may account for observed distributional patterns.

Key words: Ostracoda, habitat similarities, diversity index, Bolu, Turkey

Bolu bölgesinin (Türkiye) Ostrakotları (Crustacea) ve habitat benzerlikleri

Özet: Bolu bölgesinde 2006 yazında 144 farklı sucul sistemden 21 cinse ait 41 ostrakot toplanmıştır. Schellencandona cinsi ve 12 tür (Candona weltneri, C. sanociensis, C. lactea, Fabaeformiscandona cf. breuili, F. balatonica, F. brevicornis, F. protzi, F. latens, Schellencandona cf. belgica, Pseudocandona cf. semicognita, Potamocypris similis, P. smaragdina) Türkiye ostrakot faunası için yeni kayıttır. Ek olarak 5 tür (Herpetocypris brevicaudata, Heterocypris salina, H. rotundata, Cyclocypris laevis, Trajancypris serrata) Bolu için yenidir. UPGMA analizi Bolu’daki dokuz ilçeyi 5 gurupta göstermiştir. En fazla habitat benzerliği (% 75) Yeniçağa ve Göynük arasında bulunurken, en az benzerlik (% 20) Seben ile Merkez ilçe arasında bulunmuştur. Shannon-Weaver çeşitlilik indeksine göre Dörtdivan (0.95) eşit dağılımın en yüksek olduğu ilçe, Merkez ilçe ise indeks değerinin (H’) en yüksek olduğu ilçedir (2.63). Türlerin dağılım mekanizmaları farklıdır ve bunlar gözlemlenen dağılım şekillerine uygundur.

Anahtar sözcükler: Ostracoda, yeni kayıtlar, habitat benzerliği, çeşitlilik indisleri, Bolu

Introduction zone among the , Marmara, and Central The Bolu region plays a geographically important water bodies. Although the area supports role in species distribution as a bridge and transition different types of habitats that are home to a variety of

* E-mail: [email protected]

225 Ostracods (Crustacea) and habitat similarities in the Bolu region (Turkey)

species of plants (İkinci and Güner, 2007) and insects levels of environmental and habitat similarities (Ünal, 2000), knowledge of the region’s ostracod fauna between different species. Ostracods may indeed is limited. Earlier ostracod studies focused on species provide a sensitive biotic integrator of conditions over ecology and distributions (Külköylüoğlu, 2003, 2005a- time, and help us interpret which (if any) changes in c, 2009; Dügel et al., 2008), and none of them environmental or habitat conditions are important for attempted to compare habitat similarities either in aquatic biotas. However, this approach requires Bolu or in Turkey. Two of the most recent studies detailed knowledge about biogeographical (Külköylüoğlu and Yılmaz, 2006; Karakaş-Sarı and distribution, ecological requirements, and habitat Külköylüoğlu, 2008) attempted to compare species preferences of each species. composition and habitat similarities among different The aims of this study were to (1) contribute to the types of springs in Bolu; however, these studies failed knowledge of the ostracod fauna in the Bolu region, to represent the large-scale geographical habitat (2) analyze aquatic-habitat similarities within the similarities due to micro-habitat levels of springs. On region among 9 districts in the context of discussing the other hand, since 9 districts of Bolu are located in possible modes of ostracod dispersion, and (3) different geographical areas that possess a variety of examine the relationship between the region’s habitats and ecological conditions, there is a need to ostracod species. The list of species and ecology of understand the degree of similarities among their habitats will be provided elsewhere and available upon ostracod faunas to be able to deduce the total ostracod request. species richness of the area. Additionally, at least 4 objectives can be achieved via such knowledge of regional similarities: 1) understanding routes and Materials and methods modes of species distribution, 2) providing an Study area historical background of dispersion, 3) evaluating 2 ecological preferences of individual species, and 4) encompasses about 8301 km of estimating future possibilities of species dispersion. area, covering almost 1% of Turkey. During this study, 144 aquatic habitats including lakes, ponds, reedbeds, To evaluate these 4 objectives, an indicator-species pools, springs, and creeks were randomly selected concept has commonly been used for various from 9 districts (Merkez, , , Seben, taxonomic groups, such as plants (De Boer, 1983), Kıbrıscık, Yeniçağa, and Dörtdivan) of the province benthic invertebrates (Paine, 1969), beetles (Dufrêne (Figure 1) for sampling. and Legendre, 1997), butterflies (Launer and Murphy, 1994), amphibians (Adams, 1999), fishes (Karr, 1981), Sampling and measurement procedures birds (Beintema, 1983; Hutto, 1998), and mammals Materials were collected from different depths (up (Soulé and Terborgh, 1999). However, much remains to 100 cm of depth) between June and August of 2006 to be learned regarding application of the concept to with a standard hand-net (125 μm mesh size) and ostracods, which are small aquatic crustaceans fixed in 70% ethanol at the site. Seven major distributed across a wide range of habitats in brackish, environmental variables (pH, temperature, salinity, fresh, and saline waters. Most species have different electrical conductivity, dissolved-oxygen (and often unique) species-specific tolerance levels to concentration, redox potential, and percent oxygen a variety of environmental conditions (Külköylüoğlu saturation) were measured at the study sites before and Vinyard, 2000). Therefore, once species are sediment sampling. All samples were kept in 250 mL correctely identified in samples, the conditions in containers. In the laboratory, samples were washed habitats where species live can be estimated. This under tap water and filtered through 3 standard-sized perspective allows ostracods to be used as an indicator sieves (0.25, 1.00, 1.50 mm mesh size) and were again species to characterize water quality and other stored in 70% ethanol. A pH/ORP meter (Hanna conditions in aquatic habitats (Külköylüoğlu, 1999, model HI-98150) was used to measure pH and redox 2004), as well as habitat similarities. In this effort, potential (Eh), and an oxygen-temperature meter ostracod distributions also allow determination of (YSI- model 85) was used to measure the remaining

226 N. SARI, O. KÜLKÖYLÜOĞLU

1 2 3 4 5 6 7 8 9 42° N A 89 90 Bolu 222 40° 92 85 87 Mengen B 134 133 86 88 93 106 38° 132 135 131 96 97 115 12 136 94 95 107 C 9 128 129 41 98 10 137 130 45 44 47 111 0 200 km 11 13 40 Gerede 222 36° 126 43 42 114 26° 28° 30° 32° 34° 36° 38° 40° 42° 44° 8 Bolu 6 14 127 46 Yeniçağa 109 112 5 1 139 138 140 4 7 2 118 117 110 113 21 20 3 143 141 125 119 102 17 144 142 124 116 65 105 16 18 19 66 121 48 103 15 99 100 123 120 49 64 67 104 101 122 51 63 62 Dörtdivan 50 61 52 60 53 54 84 Mudurnu 69 Göynük 55 56 58 Seben 77 83 82 27 57 68 Kıbrıscık 26 25 59 73 76 22 39 71 78 81 28 222 24 70 74 75 80 29 31 23 38 72 79 32 37 33 36 34 35

Figure 1. Map of 144 sampling sites in the Bolu region, along with the borders of 9 districts. Each number represents a sampling site, and borders between the districts are depicted by dotted lines.

variables. Redox potential measurements were a = the number of species found in site A transformed to calculate Standard Hydrogen b = the number of species found in site B Electrode (SHE) values. Electrical conductivity (EC) values were also used to calculate Total Dissolved In order to calculate species diversity, data on the Solid (TDS), following Forester and Brouwers (1985). presence of ostracod species were analysed using the Geographical data (altitude, latitude, and longitude) following: were obtained with a global positioning system Shannon-Weaver diversity index (H') = - Σ p lnp . i i (Garmin GPS 12 XL) unit. Species identification was This includes proportions of indi viduals based on the soft body parts and carapace structures, following the systematic keys of Meisch (2000), where: Karanovic (2001, 2006) as well as the index and H' = the diversity index bibliography of non-marine Ostracoda of Kempf ln = the natural logarithm (1980, 1997). i = an index number for each species present in a Statistical analyses sample Sorenson’s Similarity Index was used to compare p = the number of individuals within a species (n ) community structures and habitat similarities of the 9 i i divided by the total number of individuals (N) present districts based on species presences following the in the entire sample. formulas below (Magurran, 1988): With these ecological applications shown above, Sorenson Similarity Index = (2c / a + b) × 100 we analyzed 2 types of biological data gathered from where; each sampling site: the number of species and the c = the number of species common in both site A number of individuals per species. The sites with the and B greatest number of species and the most equitable

227 Ostracods (Crustacea) and habitat similarities in the Bolu region (Turkey)

distribution of individuals among species are assumed UPGMA more diverse and more heterogeneous than sites with Dörtdivan few species and where 1 species is numerically Kıbrıscık Seben dominant over other species. Mengen Analyses of Unweighted Pair Group Mean Mudurnu Averages (UPGMA) were used to quantify the Gerede associations between the 9 districts of the Bolu region. Yeniçağa Sorenson’s Coefficient test was applied to the resulting Göynük UPGMA dendogram. The UPGMA analyses were Merkez performed with the Multi-Variate Statistical Package 0.25 0.40 0.52 0.64 0.76 0.88 1 Sorensen’s Coefficient - Data log(e) transformed (MVSP) version 3. 1. (Kovach, 1998). Figure 2. An analysis of Unweighted Pair-Group Mean Averages (UPGMA) shows the clustering relationships of Results ostracod fauna among 9 districts.

Forty-one ostracod taxa collected from 144 while the least similarity (the highest beta diversity) randomly located sampling stations in 9 districts were occurred between Merkez and Seben (Table 1). documented in this study. The genus Schellencandona is a new genus for freshwater habitats of Turkey. Of Shannon-Weaver diversity suggested high these, 12 species are new reports for the freshwater evenness for the 3 districts of Dörtdivan (0.95), Ostracoda fauna of Turkey. In addition to these Kıbrıscık (0.92), and Yeniçağa (0.91), whereas values of the Shannon-Weaver diversity index (H’) were species, 5 other species were documented for the first highest for Merkez (2.63), Gerede (2.36), and Göynük time in the Bolu region. Based on species binary data, (2.3) (Table 2). UPGMA showed 5 main clusters among the 9 districts (Figure 2). Table 2. Shannon-Weaver similarity index values for 9 districts The 1st group included 3 districts (Dörtdivan, in Bolu. Abbreviations include (H', Shannon index), (E, Kıbrıscık, and Seben), whereas the 2nd cluster Evenness). consisted of 1 district (Mengen), and 3rd group had 2 Name of District H' E districts (Mudurnu and Gerede). Also, 4th clustering group included 2 districts as Yeniçağa and Göynük Merkez 2.63 0.81 and the 5th group contained Merkez district. The Göynük 2.3 0.87 Yeniçağa 2.11 0.91 districts of the 4th group (Yeniçağa and Göynük) Mudurnu 1.79 0.81 showed the most similarity with each other. Seben 1.19 0.85 Kıbrıscık 2.03 0.92 According to the results of the Sorenson Similarity Mengen 2.0 0.86 Index, the greatest similarity (75%) (the lowest beta Gerede 2.36 0.87 diversity) was found between Göynük and Yeniçağa, Dörtdivan 2.1 0.95

Table 1. Percent similarities among 9 districst, calculated using the estimates of the Sorenson Index.

Location Göynük Yeniçağa Mudurnu Seben Kıbrıscık Mengen Gerede Dörtdivan

Merkez 56.41 45.71 41.17 20 29.41 34.28 55 41.17 Göynük 75 60.87 31.58 52.17 50 68.97 43.48 Yeniçağa 63.16 26.6 42.1 50 56 42.1 Mudurnu 28.58 44.4 52.63 41.6 33.3 Seben 57.14 26.6 40 42.86 Kıbrıscık 31.58 41.6 44.4 Mengen 40 21.05 Gerede 41.6

228 N. SARI, O. KÜLKÖYLÜOĞLU

Discussion and conclusion (MacArthur and Wilson, 1967), which predicts that Among the 5 clusters of districts based on species richness should increase with increasing size UPGMA, the greatest similarity of ostracod species of the sampled ‘island’. Actually, consistent results are presence (75%) based on species composition was also gained from Shannon-Weaver index (H') values between Göynük and Yeniçağa. Actually, considering (Table 2). For example, since Merkez district included the distance between these 2 districts, they are more sampling sites, its index value (H' = 2.63) is relatively far away from each other. Finding such a higher than the others, suggesting numbers of high degree of similarity, in spite of the great distance sampling sites seems to predict the values of H'. between these 2 districts, may suggest that ostracod Gerede and Göynük also had high (H' = 2.36 and H'= faunal similarity is not simply based on spatial 2.3) values following Merkez district. Shannon- proximity. In contrast, the Sorensen index showed a Weaver index may vary since species occurrence very low similarity between Mengen and Merkez changes seasonally. For example, Yiğit (2006) showed (Table 1), which was supported by the UPGMA clear seasonal differences among zooplankton analysis. Indeed, there were 9 common species populations (Cladocera, Rotifera, and Copepoda) in a between Göynük and Yeniçağa, while there were only dam lake (Kesikköprü, ) where Shannon- 6 common species between Mengen and Merkez. Weaver values fluctuated across 4 seasons. In this Among the species, Heterocypris incongruens was study, however, we did not have seasonal sampling the only species found in all 9 districts (at 54 stations) from these 9 districts and this was possibly one of the while Ilyocypris bradyi was collected from 69 stations reasons we found low levels of index values. On the in 8 districts except Dörtdivan, and Psychrodromus other hand, our finding can be a reference source for olivaceus was detected in 40 stations. These results are future studies when habitat similarities are compared. not surprising when especially the first 2 species (H. At large scales (e.g., across Turkey), our results incongruens and I. bradyi) are known as cosmopolitan demonstrate the need for more-extensive sampling of species with high tolerance levels to different freshwater organisms. Indeed, it is clear that the ecological variables (Külköylüoğlu et al., 2007). species richness of freshwater ostracods in the Bolu Psychrodromus olivaceus is also known to exhibit a region is much higher than was previously thought. wide range of distribution in the Holarctic region. In the meantime, implications of the results maybe Therefore, their high level of site occupancy in Bolu interpreted to outline a close association of habitat was found as expected. Finding 41 taxa from the region supported the idea that the region contains similarities with species diversity, in which the high levels of ostracod species diversity knowledge of indicator species (e.g., cosmopolitan, (Külköylüoğlu, 2004). Additionaly, reporting a new rare, keystone species, etc.) is a special part. Although genus and 12 new species confirms the idea of high discussion on the concept of indicator species species diversity in Turkey. However, when we continues and their selection and use require a sound compare our work with earlier reports (Altınsaçlı and quantitative database from the focal region (Carignan Griffiths, 2002), the relatively high species diversity of and Villard, 2002), local ecological data collected at ostracods within the Bolu region may also be related the regional scale should also be considered for to at least 2 main reasons: i) the lack of former studies interpreting habitat similarities. Thus, at large spatial with extensive sampling in the area limits the scope scales, ostracods can be used to explain changes due of earlier ostracod studies, and ii) high heterogenous to the deterioration of ecological integrity. geographical characteristics of the area providing variety of microhabitats for species. This also suggests that increasing the number of study sites may Acknowledgments eventually enhance the chance of finding more species We would like to thank Dr. Erik Beever from (MacArthur and Wilson, 1963, 1967). USGS Alaska Science Center for his comments and These results appear consistent with the species- help on the first draft of this work. This study was part area relationship of the Island Biogeography Theory of the MS thesis of NS.

229 Ostracods (Crustacea) and habitat similarities in the Bolu region (Turkey)

References Altınsaçlı, S. and Griffiths, H. I. 2002. A review of the occurrence and Külköylüoğlu, O. 2004. On the use of ostracods (Crustacea) as distribution of the recent non-marine Ostracoda (Crustacea) of bioindicator species in different aquatic habitats in the Bolu Turkey. Zoology in the Middle East. 27: 61-67. region, Turkey. Ecological Indicators. 4: 139-147. Adams, M. J. 1999. Correlated factors in amphibian declines: exotic Külköylüoğlu, O. 2005a. Factors effecting Ostracoda (Crustacea) species and habitat change in western Washington. J. Wild. occurrence in Yumrukaya Reedbeds (Bolu, Turkey). Wetlands. Manag. 63: 1162–1171. 25: 224-227. Beintema, A. J. 1983. Meadow birds as indicators. Environ. Monit. Külköylüoğlu, O. 2005b. Ecology and phenology of freshwater Assess. 3: 391–398. Ostracods in Lake Gölköy (Bolu, Turkey). Aquatic Ecology. 39: Carignan, V. and Villard, M-A. 2002. Selecting indicator species to 295-304. monitor ecological Integrity: A Review. Environmental Monitoring and Assessment. 78: 45-61. Külköylüoğlu, O. 2005c. Ecological requirements of freshwater Ostracoda (Crustacea) in two limnocrene springs (Bolu, De Boer, T. A. 1983. Vegetation as an indicator of environmental Turkey). Ann. Limnol. –Int. J. Lim. 41: 237-246. changes. Environ. Monit. Assess. 3: 375–380. Külköylüoğlu, O. 2009. Ecological succession of freshwater Ostracoda Dufrêne, M. and Legendre, P. 1997. Species assemblages and indicator species: the need for a flexible asymmetrical approach. Ecol. (Crustacea) in a Rheocrene spring (Bolu, Turkey). Turk. J. Zool. Monogr. 67: 345–366. 33: 1-9. Dügel, M., Külköylüoğlu, O. and Kılıç, M. 2008. Species assemblages Külköylüoğlu, O. Dügel, M., and Kılıç, M. 2007. Ecological and habitat preferences of Ostracoda (Crustacea) in Lake Abant requirements of Ostracoda (Crustacea) in a heavily polluted (Bolu, Turkey). Belgian Journal of Zoology. 138: 50-59. shallow lake, Lake Yeniçağa (Bolu, Turkey). Hydrobiologia. 585:119–133. Forester, R. M. and Brouwers, E. M. 1985. Hydrochemical parameters governing the occurrence of estuarine and marginal estuarine Külköylüoğlu, O. and Vinyard, G. L. 2000. Distribution and ecology ostracodes: an example from South Central Alaska. J. of of freshwater Ostracoda (Crustacea) collected from springs of Paleontology. 59: 344-369. Nevada, Utah, and Oregon: Apreliminary study. West. North Hutto, R. L. 1998. Using landbirds as an indicator species group. In: Amer. Natur. 60: 291-303. Avian Conservation: Research and Management. Island Press, Külköylüoğlu, O. and Yılmaz, F. 2006. Contribution to the knowledge Washington (D.C.). (eds., J. M. Marzluff, and R. Sallabanks), p. of ecological requirements of Ostracoda (Crustacea) in three 75–91. kinds of springs. Limnologica. 36: 172-180. İkinci, N. and Güner, A. 2007. Flora of Gölcük Area (Bolu, Turkey). Turk. J. Bot. 31: 87-107. Launer, A. E. and Murphy, D. D. 1994. Umbrella species and the conservation of habitat fragments: A case of a threatened Karakaş-Sarı, P. and Külköylüoğlu, O. 2008. Comparative ecology of butterfly and a vanishing grassland ecosystem. Biol. Conserv. Ostracoda (Crustacea) in two rheocrene springs (Bolu, Turkey). 69: 145–153. Ecological Research. 23: 821-830. MacArthur, R. H., and Wilson, E. O. 1963. An equilibrium theory of Karanovic, I. 2001. Meischcandona gen. now. From Africa, with a key insularzoogeography. Evolution. 17: 373-387. to the genera of the subfamily Candoninae (Crustacea, Ostracoda). Biologie. 71: 93-99. MacArthur, R. H., and Wilson, E. O. 1967. The theory of island Karanovic, I. 2006. Recent Candoninae (Crustacea, Ostracoda) of biogeography. Princeton University Press, Princeton, N.J. 203 North America. Records of the Western Australian Museum pages. Supplement. No.71. pp.75. Magurran, A. E. 1988. Ecological diversity and its measurement. Karr, J. R. 1981. Assessment of biotic integrity using fish communities. Princeton University Press, Princeton, N. J. 179 pages. Fisheries. 6, 21–27. Meisch, C. 2000. Freshwater Ostracoda of Western and Central Kempf, E. K. 1980. Index and Bibliography of Marine Ostracoda, part Europe. Süsswasserfauna von Mitteleuropa 8/3. Spektrum 1. Sonderveröffentlichungen des Geologischen Instituts der Akademischer Verlag, Heidelberg, Berlin. 522 pages. Universität zu Köln. 35: 1188. [Index A.]. Paine, R. T. 1969. A note on trophic complexity and community Kempf, E. K. 1997. Index and Bibliography of Nonmarine Ostracoda, stability. American Naturalist. 103: 91–93. part 6. Sonderveröffentlichungen des Geologischen Instituts der Universität zu Köln. 109: 1143. [Index A, Suppl.]. Soulé, M. E. and Terborgh, J. 1999. Conserving nature at regional and continental scales: a scientific program for North America. Kovach, W. 1998. Multi-variate statistical package, ver. 3.0. Kovach BioScience. 49: 809–817. Computer Services. Pentraeth, UK. Külköylüoğlu, O. 1999. Seasonal distribution of freshwater Ostracoda Ünal, M. 2000. Notes on Orthoptera of Western Turkey, with (Crustacea) in springs of Nevada. Geosound-Science and description of a new genus and four new species. J. Orthoptera Technology Bulletin on Earth Science, 35: 85-91. Res. 9: 89-102. Külköylüoğlu, O. 2003. Ecology of freshwater Ostracoda (Crustacea) Yiğit, S. 2006. Analysis of the zooplankton community by the from lakes and reservoirs in Bolu-Turkey. Journal of Freshwater Shannon-Weaver Index in Kesikköprü Dam Lake, Turkey. Ecology. 18: 343-347. Tarım Bilimleri Dergisi. 12: 216-220.

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