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Ecology and phenology of freshwater ostracods in Lake Go¨lko¨y (Bolu, Turkey) Okan Ku¨lko¨ylu¨ogˇluDepartment of Biology, Faculty of Arts and Science, Abant _Izzet Baysal University, Go¨lko¨y 14280 Bolu,Turkey (e-mail: kulkoyluoglu_o@ibu.edu.tr; phone: +90-374-253-4511; fax: +0-90-374-253-4642) Received March 23, 2004; accepted in revised form January 11, 2005 Key words: CCA, Cosmopolitan, Ecology, Ostracoda, Seasonality, Tolerance Seventeen ostracod species were recorded from Lake Go¨lko¨y (Bolu, Turkey) between January 2000 andDecember 2001. Limnocythere inopinata is a new record for the Bolu region. Canonical CorrespondenceAnalysis (CCA) explained 73% of the correlation between species and environmental variables, suggestingthat the occurrence of many species is temporally variable, and is related to seasonal changes in physico-chemical conditions. The four most frequently occurring cosmopolitan ostracod species (Candona neglecta,Darwinula stevensoni, Physocypria kraepelini, and Cypridopsis vidua) accounted for more than 70% of thespecies recorded. Water temperature, dissolved oxygen (DO), and redox potential were the most affectivevariables on the species occurrence. Two species (C. vidua, I. bradyi) were positively correlated to redoxpotential, while such a correlation was negative for P. kraepelini. The most frequently occurring species C.
neglecta was most closely related to the changes in redox potential, whereas C. vidua and D. stevensonishowed a positive correlation to water temperature. Negative strong correlation (p<0.01) was foundbetween pH and I. bradyi, but correlation was positive and weak for C. vidua. Some species (e.g. L.
inopinata) showed no clear relationship with any of those environmental variables. UPGMA clustering ofspecies based on their occurrence in different ecological conditions revealed three main species assemblages.
Analysis of species phenology using the ‘Ostracod Watch Model’ showed that temporal patterns ofoccurrence could be similar among species with similar ecological preferences. The current status of the lakeis discussed based on the present study.
nothing is known about ostracod ecology, habitatrequirements and usage in monitoring and man- In order to explain the relationship between phe- agement studies. Because physico chemical condi- nology of species and their ecological require- tions of water may vary seasonally, there is a need ments, occurrence of species is used in diverse to understand the magnitude of these seasonal ecological studies because spatio temporal patterns variations on both biotic and abiotic factors.
of species occurrence in different parts of aquatic There have been few long-term seasonal studies habitats can be influenced by seasonal variation using monthly sampling over a year in the Bolu with ecological factors (Mezquita et al. 1999a; region (Ku¨lko¨ylu¨ogˇlu 2003a, b). Some earlier Coma et al. 2000; Ramdani et al. 2001). Previous works are based on quarterly (Ku¨lko¨ylu¨ogˇlu et al.
studies (Gu¨len 1988; Ku¨lko¨ylu¨ogˇlu 1998) on 1993; Ku¨lko¨ylu¨ogˇlu et al. 1995; Ku¨lko¨ylu¨ogˇlu freshwater ostracods in Turkey were mostly 1998) or random sampling (Gu¨len 1985, 1988).
focused on their taxonomy. Consequently, almost Although these studies have made important contributions to understanding the association Canonical Correspondence Analysis (CCA) (ter between ecological factors and seasonality of Braak 1986, 1995) and Unweighted Pair Group ostracods, in general they failed to identify which Mean Averages (UPGMA) clustering frequently ecological factors were more affected by seasonal have been applied to different taxonomic assem- variations, and which factors were most closely blages (Petridis 1993), but few studies on fresh- related to the phenology of species. Since seasonal water ostracods have taken advantage of these changes in environmental variables can have direct techniques. Therefore, the aims of this study were or indirect effects on aquatic ecosystems, or both, (1) to investigate the phenology of ostracods in it is important to understand the influence of such Lake Go¨lko¨y, and (2) to examine the relationship factors on species occurrence. Little information is between environmental factors and the most fre- available on how seasonal changes affect the long- quently present species with the help of statistical term life histories of ostracod species although ostracod occurrence and phenology have beenused to draw inferences in aquatic studies,including reconstruction of the past history of habitats (Delorme 1969). This is because the tol-erance of ostracods to changes in ecological con- Lake Go¨lko¨y (40°42¢ North; 31°31¢ East, 730 m ditions does not vary over thousands of years elevation) (Figure 1) was built in a wetland area in (Smith and Forester 1994). However, until we 1970 to provide water for irrigation and other understand the ecological requirements of ostrac- agricultural uses and for commercial fishing.
ods, reconstruction of the history of habitats may Recently, the lake has been considered as an not be effective (Martens and Tudorancea 1991; alternative source of drinking water for the city of Bolu. The surface area of the lake fluctuates froman average 150 ha to a maximum of ca 180 ha.
Figure 1. Map shows nine study sites around Lake Go¨lko¨y in the Bolu (*) region.
Maximum depth of the lake is about 20 m, but Samples without ostracods were also excluded most of the lake in average does not exceed 0.1 m from the clustering and CCA analyses, in which in depth. The lake receives much of its water from only five environmental variables along with five two creeks (Mudurnu Creek from the southwest species and 24 months were selected. The mean and Abant Creek from the northeast) via concrete values of each environmental variable together canals. Additional water currently comes from one with ostracod data from nine stations were used in spring; another spring that previously fed the lake CCA for the whole lake. Detailed applications of has been closed by a concrete wall to provide how such data are introduced in cluster and/or water for public facilities around the spring CCA analyses are available in ter Braak (1995).
(Ku¨lko¨ylu¨ogˇlu 2003b). Both creeks carry nutrient Associations between species were analyzed using rich water from chicken farms, agricultural areas, UPGMA with a Jaccard Index (Ku¨lko¨ylu¨ogˇlu and villages. As a result, the lake is currently 2004). Significance values of the correlations were found from both Fisher’s r to Z tests and Pearson Materials taken from nine randomly selected correlation analyses, while pair-wise deletion was stations in the lake were collected monthly be- applied in cases of missing values. After the data tween January 2000 and December 2001 with a were log-transformed, a dendogram derived from fine plankton hand net (0.025 mm mesh size) from binary (presence/absence) data in UPGMA was shallow waters (<1 m depth) and preserved in used to show the relationships among six most glass jars (250 ml) in 70% ethanol. After ostracods common species that was encountered more than were separated from the debris and other organ- three times. All statistical analyses were conducted isms in the laboratory, they were dissected in lac- tophenol solution for identification. All species (MVSP) program version 3.1 (Kovach 1998).
were then maintained in vials in 70% ethanol.
Phenology of the four most abundant species was Both soft body parts and carapace morphology of compared with the graphical Ostracod Watch the living species were used for identification fol- Model (OWM) that aims to show cycling periods lowing systematic keys of Bronshtein (1947) and in the seasonal occurrence of species based on Meisch (2000). Organisms with damaged carap- similar ecological preference (Ku¨lko¨ylu¨ogˇlu 1998).
aces, and species represented by only one individ- All samples were stored in the Department of ual or with only juveniles were not identified to the Biology, Abant _Izzet Baysal University, Bolu.
Nine major environmental variables (water temperature, air temperature, percent oxygen sat- uration, dissolved oxygen (DO), electrical con-ductivity, salinity, total dissolved solids, pH and A total of seventeen ostracod species (Table 1) redox potential) were measured because of their were found during the 24 months of sampling. All high discriminative ability to predict species pres- species except Isocypris beauchampi (Ku¨lko¨ylu¨ogˇlu ence in previous studies (Wright et al. 1989; Ruse 2003b) were new records for Lake Go¨lko¨y. Limn- 1996). All variables were measured in situ prior to ocythere inopinata is a new report for the Bolu biological sampling from each station every region. The four most frequently occurring (n=61 month, and only the mean values were used during times) from nine stations and most abundant statistical analyses. A Hanna model HI-98150 pH/ ostracod species with more than 100 individuals in ORP meter (20°C) was used to measure redox total (i.e., Candona neglecta, Darwinula stevensoni, potential and pH. All other variables were mea- Physocypria kraepelini, and Cypridopsis vidua) sured with a YSI-85 model oxygen-temperature accounted for (22.95, 21.31, 14.75 and 11.47%, meter. Geographical data (elevation, latitude, and respectively) or 70% of all the species recorded in longitude) were recorded with a geographical the lake (Table 1). UPGMA clustering revealed clear distinctions among some species based on Relationships between species and environmen- their phenology. Some species (D. stevensoni and tal variables were examined with CCA, during C. neglecta) appeared to be eurychronal (occurring which rare species or species with no effect were almost continually throughout the year), while downweigthed in the analyses (ter Braak 1986).
some others (C. vidua and P. kraepelini) appeared Table 1. Ostracod species with their code and station numbers where they were collected in Lake Go¨lko¨y during 24 months.
Frequency (Freq. %) indicates percentage of species occurrence (or the total numbers of occurrences by means of using presence-absence data) from samples (n=61), and the star (*) represents the four most frequently occurring species that explains more than 70%of total species occurrence. Note that species codes are the same as in Canonical Correspondence Analysis.
to be stenochronal (seasonal). Based on their while the second group included only one species occurrence frequency, three main species assem- (L. inopinata), which was found four times with blages were distinguished (Figure 2). The first more than 50 individuals during summer months group included one cosmopolitan species (I. bra- (June and July) of both years. Limnocythere dyi) occurred at least three times during this study, inopinata is known to have a wide range of Figure 2. Dendogram provided from binary (presence/absence) data along with Jaccard index shows the results of UPGMA for therelationships among six most abundant species. Based on their occurrence, three main groups are clustered. First group (IB) includesone species occurred at least three times during this study. Second group includes one species (LI) found four times when third groupconsists of four cosmopolitan species (DS, CV, PK, CN) encountered more than four times that are also known from all kinds ofaquatic habitats in Turkey. Abbreviation for each species is given in Table 1.
tolerance to changes in salinity and temperature in CCA (Figure 4) suggested that species occur- both fresh and brackish water lakes. Third group rence was related to some measures of physico- consisted of four most common cosmopolitan chemical conditions (Table 2). About 73% of the species encountered more than five times with correlation between species and environment was many specimens during this study. Among the displayed with the first axis (Table 3). Total species of the third group, two good swimmer numbers of ostracod responds monthly strongly species C. vidua and P. kraepelini had similar to water temperature ( p<0.001 with 71% of spatial and temporal patterns of occurrence (Fig- correlation) and DO ( p<0.05 with a À44% of a ure 3). Indeed, both species were found in 7 of the weak correlation). Temporal changes (Figure 5) 9 sampling stations (Table 1). The other two spe- of some of the variables were similar during cies (C. neglecta, D. stevensoni) in this group are 2 years. Electrical conductivity and water tem- perature showed an inverse relationship with DO Figure 3. Graphical OWM (Ku¨lko¨ylu¨ogˇlu 1998) display phenology of the four most abundant species in Lake Go¨lko¨y during thisstudy: (a) Physocypria kraepelini and Cypridopsis vidua. (b) Darwinula stevensoni (bold arrows) and Candona neglecta (thin arrows).
The capital letters represent each month starting from January (J) to December (D).
Figure 4. CCA after joint ordination plot including five environmental variables (arrows) and five species (triangles pointed down)during 24 months (triangles pointed up). The codes for the species and the environmental factors are same as in Table 1.
Table 2. Starting from January 2000 (Ja00) to December 2001 (D01), mean values (Ave) of physico-chemical factors for each month istabulated.
pH; T(w) water and T(a) air temperature (°C); DO, Dissolved oxygen (mg/l); %S, Oxygen saturation; Sal, Salinity (ppt); EC, Electricalconductivity (lS/cm); TDS, Total dissolved solids (mg/l); Eh, Redox potential (mV); Sn, initials of the species; Sd (standard deviation,±).
Notice that about 73% of the correlations between five selected environmental variables and occurrence of five species within24 months were explained by the first two axes of the ordination diagram.
and redox potential (Eh) on the one site of the were located near the center of the ordination ordination plot. The length of vectors (arrows) diagram, probably because they have wide ran- (Figure 4) indicates the relative influence of wa- ges of tolerance to changes in environmental ter temperature, DO and redox potential, while variables such as temperature, salinity, and pH.
arrows depict the range of values of these vari- The occurrence of C. neglecta on the positive site ables in the ordination diagram. Accordingly, of Axis 1 in CCA diagram may be explained by electrical conductivity did not show any signifi- cant effect on the species occurrence. Except L. inopinata and I. bradyi, other four species J F M A M J J A S O N D J F M A M J J A S O N D Figure 5. Temporal changes in three selected variables (DO, Temp (wat), Temp (air)) and the numbers of species during 24 monthsfrom January 2000 (J00) to December 2001 for the whole lake. Notice the reverse relationship between temperature of water and air,and oxygen level of the lake that the same pattern was seen in the second year.
Table 4. Pearson correlation between five environmental variables, numbers of species (Sn), and six most abundant species analyzed.
Numbers indicate strong correlations (*p<0.05, **p<0.01) where n=24 for all variables (except for Eh and pH (n=20)). Abbrevi-ations are same as in Table 2.
this study. Occurrence patterns primarily may bedue to relationships between species phenology The ostracod fauna of Lake Go¨lko¨y does not and the location of each station and secondarily to differ markedly from that of many other lakes in seasonal variation in physico-chemical factors.
Turkey (Ku¨lko¨ylu¨ogˇlu 1998, 2003a). However, Indeed, during this study, most species were pres- patterns of species occurrence at each sampling ent in stations located on the northwest shores of location were temporally variable during the two- the lake that may suggest better aquatic conditions year study. Some species (Eucypris virens, Tonna- in those locations. This corresponds to earlier cypris lutaria, Cypris pubera, and I. beauchampi) findings. For example, distribution of ostracods were encountered only once or twice, whereas (Mezquita et al. 1999b) and oligochaetes (Petridis some others (C. neglecta, D. stevensoni, P. kra- 1993) in several aquatic ecosystems in Europe was epelini, and C. vidua) occurred repeatedly during explained by the physio-chemical characteristics of individual sites and by levels of organic pollution were mostly higher in the fall season of the second in lake water. The CCA ordination diagram year than the first one. The species occurrence was (Figure 4) shows that presence of C. vidua (and positively related to both water temperature and P. kraepelini) is closely correlated with changes in electrical conductivity (Figure 4). The phenology the conductivity (or salinity) during late summer of D. stevensoni probably reflects at least two dif- and winter months as evident on the Axis 2.
ferent and unusual life history characteristics Cypridopsis vidua, a cosmopolitan species, is one (Figure 2). First, it is ‘ancient asexual’ species of the most common species known to reflect its (Chaplin et al. 1994) with nearly continuous par- wide range of tolerance to environmental change.
thenogenetic reproduction throughout the year Although the species has two generations per year (Ranta 1979) and second, it lacks swimming setae in some locations (Kesling 1951), it has only one on its antenna, implying its inability to disperse generation per year in other locations (Mezquita actively. Although D. stevensoni is known to be et al. 2000), as is probably the case in Lake highly tolerant to variation in environmental Go¨lko¨y. In total of 39 females were mostly col- conditions in North African lakes (Ramdani et al.
lected from the stations located on the northwest 2001), it prefers high levels of oxygen to aerate the lakeshores from July to October during both years eggs and juveniles in its brood chamber. As a and only four juveniles were captured from the July result, the present study agreed with those of ear- samples of both years. This suggests that possibly lier studies (McGregor 1969) that phenology of the species might have one generation in this lake.
D. stevensoni is closely interrelated to the seasonal Physocypria kraepelini was the third most fre- quently occurring species in Lake Go¨lko¨y with about 380 individuals collected from first seven stations. Bronshtein (1947) and Ku¨lko¨ylu¨ogˇlu occurring species in Lake Go¨lko¨y. Bisexual forms (1998) have reported that this species usually is and juveniles of the species occurred from late present between early spring and the onset of February through December during both study winter, during which period, the species may years. Differences in temporal patterns of occur- complete more than one generation (Figure 3).
rence of this species reported from different geo- Absence of P. kraepelini during the winter suggests graphic locations may reflect geographic rather that the species is sensitive to low temperature and than seasonal differences in environmental factors high oxygen concentration. Seasonal variations in to which the species is sensitive (Mezquita et al.
temperature (Figure 5) may influence occurrence 1999a; Meisch 2000). The species appears to have patterns due to constraints on reproduction. Spe- a high tolerance to changes in environmental cies with similar ecological requirements should conditions in Lake Go¨lko¨y, where high level of nutrients from human and agricultural waste is a UPGMA grouped C. vidua and P. kraepelini to- problem. It appears that changes in redox poten- gether in the third group as a distinct cluster tial are closely related to the occurrence of (Figure 2). Having similar seasonal patterns of occurrence, both species are good swimmers that (Figure 4) indicates that even dramatic changes in helps them to migrate to escape unfavorable redox potential (resulting from increasing nutrient inflow to the water that causes a decline in the Another cosmopolitan species D. stevensoni was amount of DO) did not affect the occurrence of the second mostly encountered species found from this species during this study. However, even early summer (May) to late winter (December).
though individual species (as in C. neglecta) may McGregor (1969) reported the species from 12 m differ in their occurrence pattern, total number of deep waters in Gull Lake, Michigan from May to species found is related with temporal changes in October with about 2587 individuals. Compared other variables (Figure 5). For example, a reverse with earlier reports (McGregor 1969), it is the most abundant species with more than 850 individuals (p<0.01; r=0.71) and oxygen level (p<0.05; collected from seven stations around the lake r=À0.44) of the lake seemed to have an affective (Table 1). The numbers of females of D. stevensoni role on the numbers of species because the same with about six eggs observed in the brood chamber Although biotic interactions (e.g., predation, competition) were not investigated, they may also Gu¨len D. 1988. Contribution to the taxonomy of the freshwater be important determinants on the ostracod com- Ostracod Fauna of Turkey. Su U¨ru¨nleri Dergisi 1: 199–203.
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Ku¨lko¨ylu¨ogˇlu O. 1998. Freshwater Ostracoda (Crustacea) and The condition of the lake is deteriorating as a their quarterly occurrence in S¸amlar lake (Istanbul, Turkey).
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Timothy M. Uyeki,* Yu-Hoi Chong,† Jacqueline M. Katz,* Wilina Lim,† Yuk-Yin Ho,† Sophia S. Wang,* Thomas H.F. Tsang,* Winnie Wan-Yee Au,† Shuk-Chi Chan,† Thomas Rowe,* Jean Hu-Primmer,* Jensa C. Bell,* William W. Thompson,* Carolyn Buxton Bridges,* Nancy J. Cox,* Kwok-Hang Mak,† and Keiji Fukuda* In April 1999, isolation of avian influenza A (H9N2) viruses from humans wa

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