(OSTRACODA) FROM TURKEY: TAXONOMY

FIRST REPORT OF THE GENUS ISOCYPRIS (OSTRACODA) FROM TURKEY: TAXONOMY, ECOLOGY, AND GENERAL DISTRIBUTION BY 1) ˘ OKAN KÜLKÖYLÜOGLU Department of Biology, Faculty of Arts and Science, Abant Izzet Baysal University, Gölköy, TR-14280 Bolu, Turkey

ABSTRACT The genus Isocypris G. W. Müller, 1908 and its species Isocypris beauchampi (Paris, 1920) are reported for the first time from Turkey. The ecology, distribution, and taxonomic importance of this species are discussed.

RÉSUMÉ Le genre Isocypris G. W. Müller, 1908 et l’espèce Isocypris beauchampi (Paris, 1920) ont été trouvés en Turquie pour la première fois. L’écologie, la répartition et l’importance systématique de cette espèce sont discutées.

INTRODUCTION

The ostracod subfamily Isocypridinae consists of only one genus, Isocypris, including eight extant species: I. priomena G. W. Müller, 1908; I. africana (Brady, 1913); I. beauchampi (Paris, 1920); I. laskaridisi Herbst, 1951; I. longicomosa (Furtos, 1933); I. perangusta G. W. Müller, 1908; I. williamsi McKenzie, 1966, and I. devexa (Daday, 1910) (cf. Kempf, 1980, 1997; Martens, 1984; Meisch, 2000); one fossil species: I. longa (He & Zhang, 1982); and one questionable species: I. nivea G. O. Sars, 1924. Some reports on these species have been published that mention localities worldwide, e.g., Europe (Dubowsky, 1927 (in Danielopol, 1965); Bronshtein, 1947; Rome, 1947; Löffler, 1963; Ponyi et al., 1971; Kantorek, 1976; Hollwedel & Scharf, 1988; Baltanás, 1992; Meisch, 2000), Australia, North America (Delorme, 1970), South America (Martens & Behen, 1994), South Africa 1 ) e-mail: [email protected]

© Koninklijke Brill NV, Leiden, 2003 Also available online: www.brill.nl

Crustaceana 75 (9): 1083-1093

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(G. O. Sars, 1924; McKenzie, 1977; Martens et al., 1996). However, it was Triebel (1959) who has provided detailed information about important characteristics of these species, and of I. beauchampi in particular. Fox (1967) described eight species including two subspecies (I. beauchampi beauchampi and I. beauchampi cicatricosa) that are now known to be synonyms of I. beauchampi. Mastrantuono (1989), focusing on I. beauchampi, discussed the taxonomic status of the genus based on eight species in Italy. According to Mastrantuono (1989), two of the previously reported species (I. arnoldi Dubowsky, 1927 and I. nocentiniae Fox, 1963) are synonyms of I. beauchampi. However, since Mastrantuono’s (1989) study, there have been only a few reports on the taxonomy, distribution, and ecology of this species from a couple of areas. The present study constitutes the first record of the genus and of the species I. beauchampi from Turkey, since it was first described by Müller in 1908. This documentation on I. beauchampi in Turkey provides new information on the general distribution of this species. It also highlights the importance of the region as a natural bridge between Europe and Asia, as it relates to species dispersion. The rare occurrence of I. beauchampi makes it difficult to interpret its ecological preferences, especially since little is known about the ecology and life history of the species. For instance, it is unclear what level of environmental factors (e.g., temperature, pH, dissolved oxygen, salinity, etc.) I. beauchampi prefers, or what limiting factors influence its occurrence in aquatic ecosystems. Recent studies attempting to relate water quality to the types of ostracod species inhabiting certain aquatic habitats, suggest that some species may serve as useful indicators of water quality (Rosenfeld & Ortal, 1982; Eager, 1999; Mezquita et al., 1999a, b; Külköylüo˘glu, 1999, 2000; Külköylüo˘glu & Vinyard, 2000; Meisch, 2000). On the other hand, some of the non-marine ostracods are known to be sensitive to different kinds and levels of water parameters (Bromley & Por, 1975; Delorme, 1991) where ecosystem structure and functioning can be explained by means of binary data (i.e., presence-absence). Külköylüo˘glu (unpubl.) found, for example, that the presence or absence of ostracod species may provide misleading indications of water quality, when the ecology, distribution, and habitat preference of species are not well known. The aims of this study were to: (1) report the first record of the genus and species, I. beauchampi in Turkey; (2) document the species’ ecology and general distribution; and (3) discuss possible factors that account for the rare occurrence of this species in certain aquatic habitats.

MATERIALS AND METHODS

Lake Gölköy, a water storage reservoir (40◦ 42 N 31◦ 31 E) at 730 m above sea level, is located about 10 km north of the city of Bolu (fig. 1). The reservoir, with a

ISOCYPRIS FROM TURKEY

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Fig. 1. Study site (star) in the Bolu region (drawn line) in the northwestern part of Turkey.

surface area of roughly 180 hectare (average 150 ha), was built in 1970 to provide water for commercial fishing, crop irrigation, and other agricultural purposes. Recently, the reservoir has been considered an alternative source of drinking water for Bolu. As a part of an ongoing study on the ecolimnology of the lakes in Bolu, ostracods were collected with a hand plankton net (0.025 mm mesh size) from shallow waters (c. 30 cm depth) in the northwest corner of the reservoir. Ostracods have been collected on a monthly basis since January 2000, although individuals of I. beauchampi were collected only on 29 September 2000. Ostracod specimens were preserved in glass jars (250 ml) in 70% ethanol. After the specimens were separated from the debris in the laboratory, six females were collected, two of which were dissected in lactophenol solution as part of the identification process, and the rest was preserved in 70% ethanol. Both soft body parts and carapace morphology were used to identify the species. Major environmental variables (e.g., pH, temperature, conductivity, dissolved oxygen, redox potential, and percent oxygen saturation) were measured at the study site before sampling in order to avoid any pseudoreplication (see Hurlbert, 1984). A Hanna model HI-98150 pH/ORP meter (20◦ C) was used to measure redox potential and pH values, while a YSI-85 model oxygen-temperature meter was used to measure the remaining variables. Geographical data (i.e., altitude, latitude, and longitude) were recorded with a geographical positioning system (GPS-45XL) unit. Drawings were made using a camera lucida. Species identification was based on the systematic keys of Bronshtein (1947), Hartmann & Puri (1974), and Meisch (2000). In addition, the index and bibliography of non-marine Ostracoda of Kempf (1980, 1991, 1997)

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was also used. All specimens are lodged in the Department of Biology, Abant Izzet Baysal University, Bolu.

RESULTS

The genus Isocypris is a new find and hence a new addition to the known record of the Ostracoda fauna in Turkey. Six females of Isocypris beauchampi (fig. 2) were collected from the study site, with two other accompanying freshwater ostracods: Darwinula stevensoni (Brady & Robertson, 1870) (34 females), and Physocypria kraepelini G. W. Müller, 1903 (1 female). In addition, freshwater clams (family Sphaeriidae), snails (family Planorbidae), and many zebra mussels (Dreissena polymorpha (Pallas, 1771)) were collected. Isocypris beauchampi was collected only once, despite the fact that the site has been visited 22 times so far.

Fig. 2. Isocypris beauchampi (Paris, 1920). A, right valve of female, arrow = anterior; B, anterior marginal zone of right valve; C, antenna; D, uropod (furca); E, cleaning leg; F, walking leg. Scale bar: 200 µm for A, 100 µm for B, 85 µm for C-F. (A-B, original drawing (slide no.1); C-F adapted from Meisch, 2000).


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The collection of I. beauchampi expands the known range of this species to include Turkey, and emphasizes the importance of the area as a place where a rich fauna is found at the connection between Asia and Europe.

TAXONOMIC NOTES

The individuals of the species found during this study thus belong to the genus Isocypris G. W. Müller, 1908 (= Hyalocypris Brady, 1913). Comparing to most other ostracods, the females can be considered large in size (length 1.21 and height 0.34 mm, N = 2). The species can easily be recognized by the following diagnostic characteristics: valves smooth and subequal in shape, with a depression anterodorsally just in front of the eye; two relatively long setae, extending to half the length of the valves, outward on the posterior side; anterior marginal ends of both valves bear a distinct, asymmetrically shaped (denticulated) fused zone (fig. 2). This asymmetrical formation varies among adult specimens, but such information is not available for juveniles. The walking leg has two setae on the basal segment with a conspicuously long terminal claw, on which the g-seta is unusually long (a characteristic unique to this species, see Meisch, 2000). The basal segment of the cleaning leg bears three setae, while the penultimate segment ends in a pincer organ. The uropod (furca) is well developed, and has a slightly asymmetrical curve. The swimming setae on both the first and second antennae are long, exceeding the terminal claws. The terminal segment of the maxillular palp is distally enlarged and bears six bristles.

ECOLOGY AND DISTRIBUTION

Although early reports of Isocypris beauchampi exist from different parts of the world, there is little information available on its ecology and habitat preferences. This may be due to its rare occurrence (see discussion for details). I. beauchampi was first reported from the department Côte d’Or in France (Paris, 1920). In lentic habitats, Marmonier & Creuzé des Châtelliers (1992), and Creuzé des Châtelliers & Marmonier (1993) found the species in slightly eutrophic and slow-flowing interstitial waters of the river Rhône. This rare species was subsequently reported with about 10 individuals from the running waters of the Michelsbach and from stagnant waters (in a dry meander-belt with loam-pits) within the nature reserve ‘Hördter Rheinaue’ (Scharf, 1988), and from a mesotrophic-eutrophic lake, Lake Holzmaar in Germany (Scharf, 1993). The species has also been found in rice fields near Nora, Italy (Fox, 1963). According to Baltanás (1992), a population of this species was present in the slow flowing portion of the river Jarama

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(Iberian Peninsula) where aquatic macrophytes were present. In addition to these studies, some data suggest that I. beauchampi prefers the stagnant littoral zones of lakes: for instance, about 50 females were reported at a depth of 6-9 meters in a hydroelectric lake-reservoir located at 1300 m altitude in Campotosto, Italy (Mastrantuono, 1989). In Britain, Fox (1967) found adult females with eggs and also larvae of the species in October. Similarly, in the present study, two of the females were found with eggs but not with larvae. Danielopol et al. (1985, 1988), and Danielopol (pers. comm.) found the species in the meso-eutrophic lakes of Mondsee (Austria) and Salzburg (upper Austria). Meisch (1990) measured conductivity values (580 µS/cm) from a pond called Etang S.E.O. in Luxembourg. Meisch (1990) also measured other variables from this site, and listed some that are commonly used to identify water quality: nitrate (NO3 ) < 1.0 mg/l, ammonium (NH4 ) < 0.1 mg/l, and phosphate (P) < 0.1 mg/l. Accordingly, all of these three variables are apparently below the threshold values as described by the American Public Health Association (APHA, 1985). Thus, based on these values provided by Meisch (1990), the water in this pond where I. beauchampi was reported can be characterized as oligotrophic. An important study on the environmental requirements of I. beauchampi in rivers was conducted in the Cuenca Mountains in Central Spain (Mezquita et al., 1996). Those authors collected the species in August at 950 m a.s.l., and documented environmental data about the localities where the species was found. These authors measured conductivity (747 µS/cm), percent oxygen saturation (93%), dissolved oxygen (7.5 mg/l), pH (8.32), and water temperature (20.5◦ C) from muddy parts of the river with fine particulate organic matter. This study is significant in that it takes into consideration some of the major environmental factors, which can be useful in interpreting possible relationships between the occurrence of I. beauchampi and the conditions past and present of its aquatic habitat. Most recently, Mezquita et al. (1999a) noted the importance of using ostracod occurrences as an indirect indicator of water quality, and as part of any monitoring system for the subsequent management of streams. In particular, the authors suggest that the occurrence of I. beauchampi along with that of an accompanying species, Potamocypris variegata (Brady & Norman, 1889), might be correlated with streams at low altitudes that have a relatively high water discharge, dissolved chloride, and organically enriched warm waters, all of which suggest poor water quality. According to Mezquita et al. (1999a), individuals of the species were collected from April to November (July-September not included) between 61 m (Millars river) and 700 m a.s.l. (Xúquer river) on the eastern Iberian Peninsula. This present study also measured some of the major water variables such as electrical conductivity (263 µS/cm), dissolved oxygen (10.08 mg/l), oxygen saturation (110.3%), water temperature (19.3◦ C), and salinity


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(0.1 ppt). Redox potential and pH values were not measured from this site during sampling, but average (N = 15) pH and Eh values were known from the ongoing study (Külköylüo˘glu, unpubl.) as 8.04 and −63.15 mV, respectively. I. beauchampi occurs mostly in warm-stagnant waters, so that the species is labelled as a warmstenothermal species by Nüchterlain (1969), and also described as oligorheophilic and oligohalophilic by Meisch (2000).

DISCUSSION

The ecology and habitat preferences of Isocypris beauchampi are not well known, despite early records, which is possibly due to the rare occurrence of the species, its phenology (seasonality), and because little information is available on the major water parameters of its habitat. The presence or absence of I. beauchampi can be related to its phenology in addition to several environmental factors within its habitat. Indeed, early studies suggest that some species are seasonal in their occurrence and, therefore, a single collection may not provide representative data on the occurrence of the present species in a given locality. Consequently, finding I. beauchampi at one location and at one time does not necessarily represent the overall species diversity or distribution. For example, many species of the genus Eucypris generally occur during winter (Külköylüo˘glu, 1998) whereas the ‘ancient asexual’ species (Chaplin et al., 1994) D. stevensoni can be found throughout the year (Ranta, 1979). Therefore, if species, for example, are not collected during the winter season (often due to unfavourable weather conditions), this does not necessarily imply that the species are not present in that particular habitat. In terms of I. beauchampi, this species seems to occur in relatively low numbers from April to December. Failure to take into account the phenology of I. beauchampi and other ostracod species can lead to a misinterpretion of the data regarding species density and distribution. This should be an important consideration in any longterm biomonitoring study and in any subsequent management implications. The use of indicator species has been proposed over a hundred years ago as an efficient method to understand past and present, as well as to forecast future conditions of aquatic habitats (Kolkwitz & Marsson, 1908; Cairns & Pratt, 1993). However, without complete knowledge of a species (e.g., its phenology), interpretation of the results can be misleading. For example, when we looked at associated ostracod species (Darwinula stevensoni and Physocypria kraepelini), several freshwater clams (family Sphaeriidae), snails (family Planorbidae) and chemical data, the results suggested that the aquatic habitat was of good quality. However, more detailed studies are needed to test the reliability of using ostracods as indirect indicators of water quality. Thus, even though studies utilizing indicator

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species to explore environmental conditions are available, many researchers prefer to use more direct chemical and physical measurements to reduce any possible misinterpretion of species presence or absence, and to better understand what the species’ occurrence can tell about its aquatic habitat. At present, some information is available for a few ostracod species, and while there are some ecological and environmental data for Isocypris beauchampi, clearly more research is needed before the species can potentially be used as an indicator of water quality, or before the species can be used to classify the waters in which it occurs. Knowledge of ostracod species may also be useful in reconstructing the history of an environment, but only a few fossils of I. beauchampi have been collected in Germany (Scharf et al., 1995) and thus it is difficult to explain the past of an area by relying solely on this species. Instead, it is suggested, by this study, that species such as I. beauchampi may be useful in explaining past environmental conditions as long as recent data are examined, in addition.

ACKNOWLEDGEMENTS

I would like to thank Dan L. Danielopol (Mondsee, Austria) and Koen Martens (KBIN, Brussels) for their helpful comments on the earlier manuscript, and Patrick De Deckker (ANU, Australia) for kindly sending me important papers. My special thanks are given to Dean Kinerson (BLM, U.S.A.) for his help in English and valuable suggestions, and Eriman Topba¸s (Abant ˙Izzet Baysal University, Turkey) for his help in the French translation on the first draft of this manuscript. Also, with my sincere appreciation, Erdo˘gan Usta (Abant ˙Izzet Baysal University, Turkey) must be acknowledged for his encouragement and tremendous help during sampling.

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First received 29 December 2001. Final version accepted 2 July 2002.