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Taxonomy, distribution, and ecology of crustacean zooplankton in trough waters of Ankara (Turkey)

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http://journals.tubitak.gov.tr/zoology/ © TÜBİTAK

doi:10.3906/zoo-1301-7

Taxonomy, distribution, and ecology of crustacean zooplankton in trough waters of Ankara (Turkey)

Elif BAŞAK1,*, Cem AYGEN2, Okan KÜLKÖYLÜOĞLU1

1Department of Biology, Faculty of Arts and Science, Abant İzzet Baysal University, Gölköy, Bolu, Turkey

2Department of Marine-Inland Water Sciences and Technology, Faculty of Fisheries, Ege University, Bornova, İzmir, Turkey

1. Introduction

Artificial habitats have increased in number rapidly due to human activities, dramatically affecting natural habitats. For example, they can cause habitat and species loss (Külköylüoğlu, 2003). Troughs are one example of artificial structures that alter natural water bodies to artificial forms. They are built by converting springs or groundwater (Külköylüoğlu et al., in press). Troughs are used to store water for animals and drinking water for villagers, and for irrigation. Modification of a water body by using an artificial structure is a common method for increasing biodiversity in fresh or marine waters (Bulleri and Chapman, 2004; Burt et al., 2009). Artificial reefs, for example, are made from truck tires or concrete blocks (Lim et al., 1976), and from sticks, poles, and bundles of brushes (Polovina, 1991) to increase fish diversity. Artificial beds constructed from plastic lead to increases in the growth of macro-algae (Godoy and Coutinho, 2002). Considering troughs, there is a single study, by Külköylüoğlu et al. (in press), who investigated the distribution and ecology of Ostracoda from trough waters. However, there is no study

about the effect of troughs on zooplankton biodiversity.

If troughs support diversity for animals and plants, they could be called “artificially natural habitats” (Külköylüoğlu, pers. comm.).

Zooplanktons are small microscopic organisms that can inhabit a variety of aquatic habitats. They have an important position in aquatic food chains as energy transmission from primary producers to the top trophic levels, i.e. predatory fishes and marine mammals (Sommer and Stibor, 2002). Zooplanktons are affected by environmental conditions and can rapidly respond to environmental changes (Dodson and Frey, 2001;

Williamson and Reid, 2001; Dodson et al., 2005).The 3 main groups of zooplanktons are Rotifera, Cladocera, and Copepoda. In this study, we worked with 2 groups (Copepoda and Cladocera).

As far as we know, there has been no extensive geographical study on the zooplankton composition of the troughs, as much of the knowledge about zooplanktons is confined to specific locations or habitats. Thus, this is actually the first extensive study on zooplanktons Abstract: Troughs are one of the main components of villages in Turkey. They are constructed by converting springs or underground waters. Until now, there has been no extensive study investigating the composition and diversity of trough zooplankton species. In order to contribute knowledge on the zooplanktons in troughs, 142 troughs were randomly sampled from 17 districts in Ankara Province between 22 June and 3 July 2011. A total of 18 zooplanktons including 11 Copepoda and 7 Cladocera species were determined. Twelve of the 18 (Paracyclops chiltoni, Paracylops fimbriatus, Paracyclops imminutus, Tropocyclops prasinus, Diacyclops bisetosus, Acanthocyclops vernalis, Canthocamptus staphylinus, Attheyella crassa, Bryocamptus minutus, Macrothrix hirsuticornis, Oxyurella tenuicaudis, Moina macrocopa) are new records for Ankara. Paracyclops imminutus was reported for the third time in Turkey in the last 50 years. UPGMA illustrated 4 main clustering groups of species corresponding to some of their ecological characteristics. Poisson distribution analysis showed almost random distribution of species among the troughs (s2/µ = 1.04). With their cosmopolitan characteristics, 3 species (M. hirsuticornis, E. serrulatus, and C. sphaericus) are the most common species. Their ecological tolerance and optimum values were higher than the mean tolerances for different environmental variables. The results show that troughs may provide suitable conditions for zooplankton species.

Key words: Copepoda, Cladocera, trough, distribution, ecology, Poisson distributio

Received: 05.01.2013 Accepted: 20.05.2013 Published Online: 01.01.2014 Printed: 15.01.2014

Research Article

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inhabiting troughs. The aims of this study are: 1) to determine the zooplankton fauna of troughs in the Ankara region, 2) to contribute knowledge on zooplankton ecology and diversity, and 3) to emphasize the similarity between troughs and their species composition.

2. Materials and methods

Ankara Province is situated in the Central Anatolia region (39°55′15.0054″N and 32°51′14.8062″E, 938 m a.s.l.); it is of about 25,207 km2 surface area. A total of 142 troughs (Table 1) were randomly sampled between 22 June and 3 July 2011 from 17 districts in Ankara Province (Figure 1).

Selection of troughs was based on the ratio of the surface area of each district, so that the bigger the area, the higher the numbers of stations and troughs (e.g., for an area with a size of 0–1000 km2, 5 stations were selected; when the area was about 1000–2000 km2, 10 stations were selected;

if the area was equal to or more than 2000 km2, 15 stations were selected).

Depth (D, m), width (W, m), and length (L, m) were measured by a standard meter. Water temperature (Tw,

°C), electrical conductivity (EC, µS/cm), salinity (Sal, ppt), pH, specific electrical conductivity (SPEC, µS/

cm), dissolved oxygen (DO, mg/L), percent oxygen saturation (%DO), total dissolved solid (TDS, mg/L), and atmospheric pressure (atm, mmHg) were measured using a YSI Professional PlusMulti parameter. Geographical data (altitude [alt] and coordinates) were obtained by using a Garmin GPS 12 XL. An anemometer (Testo 410- 2 model) was used to measure air moisture (MOI), wind speed, and air temperature. After the ecological variables were measured, the zooplankton samples were collected in 250-mL plastic jars and fixed with 70% alcohol. In the laboratory, samples were washed under water and filtered through 500-µm–sized sieves to separate Rotifera. Under stereomicroscope, both groups of cladoceran and copepod samples were separated into different vials and fixed with 70% ethanol. Borutskii (1964), Dussart (1969), Einsle Table 1. Species and station numbers where species were found.

Species Station numbers where species found

Eucyclops serrulatus (Fisher, 1851) 3, 4, 8, 9, 11, 12, 15, 20, 22, 24, 25, 26, 30, 34, 37, 38, 39, 41, 44, 46, 47, 49, 50, 55, 56, 57, 66, 67, 68, 73, 76, 79, 81, 83, 93, 96, 100, 101, 104, 105, 106, 108, 109, 110, 111, 112, 113, 121, 123, 124, 125, 127, 129, 130, 131, 133, 135, 137, 138, 139, 140, 141, 142 Paracyclops chiltoni (Thomson, 1882) 1, 19, 22, 25, 33, 43, 46, 48, 58, 59, 84, 89, 94, 106

Paracyclops fimbiratus (Fisher, 1853) 9, 15, 39, 53, 60, 66, 68, 83, 85, 87, 90, 98, 114, 133, 138, 140, 141, 142 Paracyclops imminutus (Kiefer, 1929) 114

Tropocyclops prasinus (Fisher, 1860) 8 Diacyclops bisetosus (Rehberg, 1880) 29 Acanthocyclops robustus (G. O. Sars, 1863) 40, 135 Acanthocyclops vernalis (Fisher, 1853) 73, 75, 122

Canthocamptus staphylinus (Jurine, 1820) 3, 39, 40, 112, 122, 135

Bryocamptus minutus (Claus, 1863 15

Attheyalla crassa (Sars, 1862) 12, 112

Moina branchiata (Jurine, 1820) 119

Moina macrocopa (Straus, 1820) 20

Macrothrix hirsuticornis (Norman and Brady, 1867) 7, 8, 10, 12, 14, 15, 19, 20, 21, 22, 24, 25, 28, 39, 48, 49, 67, 74, 103, 104, 106, 110, 111, 112, 114, 123, 130, 140, 142

Pleuroxus aduncus (Jurine, 1820) 19, 44, 123, 130

Chydorus sphaericus (O.F.Müller, 1776) 7, 24, 25, 30, 39, 44, 46, 57, 71, 73, 78, 84, 90, 92, 106, 107, 109, 110, 111, 112, 116, 124, 126, 138

Leydigia leydigi (Schoedler, 1863) 102, 135 Oxyurella tenuicaudis (Sars, 1862) 9, 25, 53, 60

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(1996), Karaytuğ (1999), Dussart and Defaye (2001), and Wells (2007) were used to identify copepods. The taxonomic key by Flösner (1972) was used for cladocerans.

For statistical analysis, 12 species were used that occurred at least 3 times, along with the 10 most important environmental variables (depth, width, length, altitude, moisture, water temperature, electrical conductivity, pH, dissolved oxygen, and atmospheric pressure). To obtain the normal distribution of variables, the raw data were log (e) transformed whenever necessary.

Unweighted pair group method with arithmetic mean (UPGMA), applied by using MVSP version 3.1 (Kovach, 1998), was used to show a possible clustering relationship among the 12 zooplankton species (Eucyclops serrulatus, Paracyclops chiltoni, P. fimbiratus, Acanthocyclops robustus, A. vernalis, Canthocamptus staphylinus, Attheyella crassa, Macrothrix hirsuticornis, Chydorus sphaericus, Pleuroxus aduncus, Oxyurella tenuicaudis, Leydigia leydigi).

Nonparametric Spearman correlation analysis, evaluated with SPSS (version 11.01), was used to understand the relationships between 10 physiochemical environmental variables and 12 species. Species optimum estimates and tolerance ranges were calculated by using the C2 program (Juggins, 2003). To investigate the correlation between

altitude and species, a bar graph was drawn by dividing altitudes into 100-m intervals. The class interval was determined by selecting class width. Accordingly, class interval should be between 10 and 20 (the range should be at least 10 class intervals but not more than 20). There are 142 stations, and when divided by 10, the result is 14.2, which is suitable.

The Poisson distribution model was used to determine the types of population dispersion.

Poisson probability can be calculated based on the formula below:

( ) !µ P x exµ x

=

where x is the number of occurrences of an event, µ is the mean number of successes that occur in a specified region, and e is the constant value, equal to 2.71828. Values of Poisson probability were tested with the chi-square test.

Accordingly, distribution of species was determined based on the ratio between variance and mean (s2/µ). If the ratio (s2/µ = 1) is 1, distribution is random; (s2/µ > 1) indicates clumped distribution; (s2/µ < 1) indicates uniform distribution (Ludwig and Reynolds, 1988).

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31°00"E 32°00"E 33°00"E 34°00"E

30°00"E

39°00"N40°00"N

5.

N

TURKEY

Figure 1. The map illustrates 142 trough sites sampled in Ankara.

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3. Results

In this study, 11 Copepoda species and 7 Cladocera, in total 18 species, were reported from 99 troughs at 142 stations (Table 1). A total of 12 species were newly recorded for Ankara: Paracyclops chiltoni, P. fimbiratus, P. imminutus, Tropocyclops prasinus, Diacyclops bisetosus, Acanthocyclops vernalis, Canthocamptus staphylinus, Attheyella crassa, Bryocamptus minutus, Macrothrix hirsuticornis, Oxyurella tenuicaudis, and Moina macrocopa. This is the third time that P. imminutus has been recorded for Turkey. The most common species was Eucyclops serrulatus, with 63 occurrences, while Macrothrix hirsuticornis was collected 29 times, and Chydorus sphaericus was collected 24 times.

Six species (T. prasinus, D. bisetosus, P. imminutus, B.

minutus, M. macrocopa, and M. branchiata) were the least-collected species with 1 occurrence each. Based on the UPGMA dendrogram, 12 zooplankton species were clustered into 4 main groups (Figure 2). Results of Spearman correlation (Table 2) and UPGMA analyses were partially supportive of each other. According to tolerance optimum values applied on zooplanktons for the first time (Table 3), ecological tolerance and optimum estimations for species were variable. Some species have a higher value for both tolerance and optimum estimates than the mean. Results of Poisson analysis (P = 0.05, N >

30) showed that species were almost randomly distributed among troughs (s2/µ = 1.04) (but see Discussion). The

graph drawn according to the frequency distribution table (Figure 3) supports our results (see Ludwig and Reynolds, 1988, p. 20). To investigate the correlation between altitude and species, a graph was drawn by dividing altitudes into 100-m intervals (Figure 4). As a result of this, altitude did not have a significant effect on species number.

4. Discussion

The most frequently occurring 3 species, Eucyclops serrulatus, Macrthrix hirsuticornis, and Chydorus sphaericus, were also the most abundant and dominant species. These species have a broad geographical distribution in natural systems and wide ecological tolerance to environmental variables (Miracle, 1982). In the present study, we collected them from 63 (E. serrulatus), 29 (M. hirsuticornis), and 24 (C. sphaericus) different troughs. These 3 species were frequently found together in troughs. In contrast, in the UPGMA dendrogram, only E. serrulatus and M. hirsuticornis were clustered in a single group. The reason for this probably lies in the difference in the tolerances of the individual species to the various environmental variables. For almost all of the variables, these 3 species tend to have greater tolerance levels than the mean value (Table 3). This probably gives an advantage to them in existing in a wide range of conditions. On the other hand, none of these species showed significant correlations to other variables (Table 2). This may suggest

UPGMA

Spearman Coefficient - Data log(e) transformed

EU ATT MH

PA PC CS AR CAN LL AV PF

-0.2 0 0.2 0.4 0.6 0.8 1

OT I

III II

IV

Figure 2. UPGMA illustrates the clustering relationships of 12 zooplankton species.

Abbreviations: EU: Eucyclops serrulatus; PC: Paracyclops chiltoni; AR: Acanthocyclops robustus; PF: Paracyclops fimbiratus; AV: Acanthocyclops vernalis; MH: Macrothrix hirsuticornis; CS: Chydorus sphaericus; PA: Pleuroxus aduncus; OT: Oxyurella tenuicaudis; LL: Leydigia leydigi; CAN: Canthocamptus staphylinus; ATT: Attheyalla crassa.

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Table 2. Spearman correlation shows the relationships among the environmental variables and species. n = 97; “(a)” marked where n = 93. “*” correlation is significant at the 0.05 level (2-tailed) and “**” correlation is significant at the 0.01 level (2-tailed). Depth and length did not show any significant correlation between environmental variables and species. Abbreviations: W: weight; ALT: altitude; MOI: moisture; TW: water temperature; EC: electrical conductivity; pH; DO: dissolved oxygen; ATM: atmospheric pressure; EU: Eucyclops serrulatus; PC: Paracyclops chiltoni; AR: Acanthocyclops robustus; PF: Paracyclops fimbiratus; AV: Acanthocyclops vernalis; MH: Macrothrix hirsuticornis; CS: Chydorus sphaericus; PA: Pleuroxus aduncus; OT: Oxyurella tenuicaudis; LL: Leydigia leydigi; CAN: Canthocamptus staphylinus; ATT: Attheyalla crassa WALTMOITWECpHDOATMEUPCARPFAVMHCSPAOTLLCANATT W1.000 ALT0.040(a) 1.000 MOI–0.0980.078(a) 1.000 TW0.059–0.316**(a)–0.424**1.000 EC–0.025–0.305**(a)–0.0160.0921.000 pH–0.100–0.406**(a)–0.297**0.540**–0.0211.000 DO0.014–0.025(a)–0.363**0.549**–0.0720.557**1.000 ATM–0.034–0.898**(a)–0.1030.387**0.356**0.345**0.0591.000 EU0.0340.095(a)0.120–0.117–0.110–0.239*–0.029–0.0671.000 PC0.127–0.185(a)–0.322**0.261**0.1310.219*0.212*0.266**–0.252*1.000 AR0.1370.228*(a)–0.150–0.1400.019–0.1080.017–0.224*–0.052–0.0621.000 PF–0.212*0.091(a)0.062–0.1200.053–0.150–0.076–0.0890.018–0.120–0.0691.000 AV–0.0530.168(a)0.267*–0.1970.166–0.116–0.222*–0.178–0.127–0.076–0.026–0.0851.000 MH0.0600.253*(a)–0.0270.010–0.138–0.1260.185–0.1910.0920.069–0.093–0.028–0.1141.000 CS–0.0480.137(a)0.0120.000–0.208*0.0310.060–0.1980.0490.097–0.082–0.0960.049–0.0251.000 PA–0.0600.001(a)0.0610.034–0.0020.0660.0700.0190.0700.065–0.030–0.098–0.0370.252*0.0071.000 OT–0.1300.056(a)–0.0850.170.190–0.0360.0890.086–0.0680.0430.0300.302**–0.037–0.025–0.007–0.0431.000 LL0.1880.002(a)–0.088–0.1190.077–0.162–0.1640.003–0.054–0.0620.489**–0.069–0.025–0.093–0.082–0.030–0.0301.000 CAN0.0580.295**(a)–0.131–0.1370.006–0.1770.110–0.335*0.0390.0120.571**0.0060.204*–0.0140.052–0.053–0.0530.251*1.000 ATT–0.1470.054(a)0.123–0.014–0.003–0.1510.101–0.0850.164–0.062–0.021–0.069–0.0260.218*0.087–0.030–0.030–0.0210.251*1.000

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Table 3. Optima (uk) and tolerance (tk) values are calculated for the mean depth (D), altitude (ALT), water temperature (Tw), electrical conductivity (EC), pH, dissolved oxygen (DO), and atmospheric pressure (ATM). N2 shows Hill’s coefficient (measure of effective number of occurrences). Count and Max represent numbers of species occurrence and numbers of individuals. Abbreviations: MOI: moisture; EC: electrical conductivity; pH; DO: dissolved oxygen; ATM: atmospheric pressure. SpeciesCountMaxN2DALTMOITwECpHDOATM uktkuktkuktkuktkuktkuktkuktkuktk E. serrulatus63111411.0830.320.17988.2254.5542.4220.1218.174.11536.12713.077.990.6610.172.93672.1710.14 M. hirsuticornis2929810.4410.400.171028.7264.5137.4816.7118.242.84634.44542.707.132.2411.263.45669.465.74 P. chiltoni15218.8020.350.19952.38224.0926.187.5619.712.78633.33574.577.930.3410.633.00680.0516.61 P. fimbriatus18563.3800.300.09448.76661.3535.257.8517.092.13460.56797.027.270.629.492.71665.6815.19 C. sphaericus247043.3660.350.221048.3278.1640.469.3616.653.03194.89240.738.170.7210.602.67670.3222.38 C. staphylinus6122.90440.450.201388.4126.6925.5321.8216.203.22451.30155.587.680.3211.311.50645.427.49 P. aduncus4572.07460.160.161107.5189.6541.6642.2022.098.61495.41132.168.190.7411.192.21670.1811.69 O. tenuicaudis4841.56860.290.051027.3167.0520.7810.5720.811.65900.0411876.78.030.4210.781.83672.618.70 Mean0.330.16998.72270.7633.7217.0216.623.55538.26629.077.800.7610.682.54668.2412.27 Max.0.450.221388.4661.3542.4242.2022.098.61900.041876.78.192.2411.313.45680.0522.38 Min.0.160.05448.76126.6920.787.5616.201.65194.89132.167.130.329.491.50645.425.74 St. dev.0.0850.056259.84166.138.382611.5942.08492.1699200.9563.70.40520.62080.61920.649210.085.4878

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that species with high tolerances to different environmental variables do not need to display a direct correlation to those variables due to cosmopolitan characteristics.

Indeed, this view has already been supported by ostracods, but the results cannot be generalized for zooplanktons (Külköylüoğlu, pers. comm.).

The maximum number of species in a trough was 6 when all of them were cosmopolitans. Similarly, Uçak (2012) reported a maximum of 5 ostracod species per trough when most of the species had cosmopolitan characteristics. These results may correspond with the idea that troughs, as artificial structures, can be dominated by cosmopolitans first in ecological succession. However, since most of the troughs are cleaned up from time to time, there is no further increase in the levels of such succession.

Troughs are very useful structures for villagers and animals in many ways (Figure 5). They are frequently cleaned and filled by villagers. Drenner et al. (2009) reported that zooplankton species are recolonized after lentic systems are filled by rainfall. Similarly, some troughs are filled up by rainfall (but not all). After troughs are refilled, zooplankton species can reappear within a couple of days or weeks. This cleaning process may be one of the reasons that a low number of different species were found in some troughs, suggesting that there might be not enough time to recolonize. Among zooplanktons, rotifers and copepods are faster colonizers in the new water habitats than cladocerans (Badosa et al., 2010). Frisch and Green (2007) also concluded that cyclopoid copepods, especially the Eucylops and Tropocyclops genera, were early colonizers with the capacity to colonize the water column after rehydration. In the present study, species numbers of copepods (mostly cyclopoid copepods) were higher than cladocerans, and so colonization rate might have a role in this. Additionally, we did not find any calanoid copepods.

Not having enough time to colonize might be one possible

explanation for the absence of calanoids. Another possible reason might be different habitat preferences of species.

Calanoid copepods can be found in many kinds of water bodies: for example, from temporary ponds in Iceland (Scher et al., 2000), in Antarctica (Pugh et al., 2002), in cave waters (Brancelj, 2005; Brancelj and Dumont, 2007), and lakes and rivers (Bozkurt, 2004; Yiğit, 2006; Atici et al., 2008). However, calanoid copepods are planktonic organisms, while cyclopoid and harpacticoid copepods prefer substrates in littoral or benthic habitats (Galassi et al., 2009). Another difference between cyclopoid copepods and calanoid copepods is that calanoid copepods are generally predominant in oligotrophic conditions, while cyclopoid copepods are suited and well adapted to eutrophic conditions (Gannon and Stremberger, 1978; Kaya and Altındağ, 2007;

Aygen et al., 2009). Based on this information, troughs can be considered as eutrophic habitats when some indicator species (e.g., Chydorus sphaericus, Eucyclops serrulatus, and Acanthocyclops robustus) are found in them (Bekleyen and Taş, 2008; Özdemir Mis and Ustaoğlu, 2009).

Stoch (2007) reported that in high-altitude environments above 2700 m, copepod species richness is low, but higher species richness was common from 1100 and 2700 m. Figure 4 represents relationships between numbers of species and troughs at different altitudinal ranges. Thus, it seems that species number increased with altitude. At the same time, the numbers of troughs also increased; this might be a possible reason for finding high numbers of species at high altitudes.

After calculating the variance and mean values, we defined the ratio of s2/µ = 1.04 for the Poisson distribution.

As we mentioned above, according to Ludwing and Reynolds (1988), if this ratio equals 1, the distribution pattern is random; if it is smaller than 1, the distribution pattern is uniform; and if the ratio is greater than 1, the distribution pattern is clumped. After all, 1.04 is very

43

54

21 18

3 3

0 10 20 30 40 50 60

0 1 2 3 4 5+

Numbers of troughs

Numbers of species per sample

0 5 10 15 20 25 30 35

Value

Range (m) Species no.

Trough no.

400–50 0 501–60

0 601–700701–80

0 801–90

0 901–100

0

1001–12001201–13001301–14001401–1500 1001–1100

Figure 3. Distribution of the numbers of species among 142 troughs from no species (0) in 43 troughs to 5 (5+) or more species in 3 troughs.

Figure 4. Number of species (species no.) and numbers of troughs (trough no.) at 100-m altitudinal ranges.

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close to 1. Therefore, we decided that the zooplankton distribution pattern among troughs is random, as a small difference (0.04) can be ignored.

Troughs are built by converting springs because the usage of them is very important and useful for villagers.

Despite the original species composition of the spring habitat being affected by the springs’ conversion into troughs, troughs may provide suitable conditions for some aquatic species, especially for cosmopolitan species.

On the other hand, some rare species may have a chance to survive in troughs because troughs can provide possibilities. Nevertheless, to have a better understanding

about the importance of troughs for biodiversity, further studies on different taxonomic groups are needed.

Acknowledgments

We are grateful to Prof Dr Süphan Karaytuğ (Mersin University) and Dr Didem Özdemir Mis (Ege University) for their help during taxonomic investigations. Also, we acknowledge Dr Derya Akdemir and Samet Uçak for their help during fieldwork. In addition, we would like to thank DSİ Assistant General Manager Döndü Tatlıdil and Hüseyin Kaya for their help in providing a vehicle during our fieldwork.

Figure 5. a) trough with 4 segments made of cement (photo

taken 23 June 2011). Figure 5. b) trough made of carping oak tree (photo taken 27

June 2011).

Figure 5. c) trough made of cement (photo taken 24 June 2011). Figure 5. d) trough used by goats (photo taken 25 June 2011).

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