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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: email@example.com; 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 (l
S/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,
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