Hydrobiologia 452: 101–107, 2001.
© 2001 Kluwer Academic Publishers. Printed in the Netherlands.
101
Temporal occurrence of Ceratium hirundinella in Spanish reservoirs
C. Pérez-Martı́nez1,2 & P. Sánchez-Castillo1,2
Institute of Water Research, Ramón y Cajal 4, University of Granada, 18071 Granada, Spain
2 Dpto. Biologı́a Animal y Ecologı́a, Facultad de Ciencias, Universidad de Granada, 18071 Granada, Spain
E-mail: [email protected]
Received 10 July 2000; in revised form 16 January 2001; accepted 19 February 2001
Key words: Ceratium hirundinella, ionic content, reservoir, temporal occurrence, temperate zone
Abstract
Ceratium hirundinella has traditionally been characterised as a species that thrives in warm waters and in stratified
conditions. In our study, however, we found that the temporal occurrence of C. hirundinella in Spanish reservoirs
greatly differs from that typically described in temperate zone aquatic systems. We analysed the temporal occurrence of C. hirundinella populations as well as physical and chemical variables in one hundred Spanish reservoirs.
C. hirundinella was present in most (74%) of the reservoirs. In 78% of the reservoirs with C. hirundinella occurrence, the species was present during winter time and in 70% it was present during all four seasons.C. hirundinella
was very commonly present in Spanish reservoirs in winter time despite the mixing conditions and lower temperatures and light availability. The presence of the species was positively related to water ionic content (HCO3 − ,
SO4 2− , Ca2+ , Mg2+ ). We conclude that C. hirundinella temporal occurrence in southern north-temperate systems
greatly differs from the seasonality typically described for the temperate zone and could be regulated by different
factors than those operating in the northern north-temperate zone.
Introduction
Ceratium hirundinella is a common phytoplanktonic
species in the stratified and warm waters of temperate
lakes and reservoirs at the end of the summer period
(Nauwerck, 1963; Tamás, 1974; Heaney, 1976; Reynolds, 1976; Barko et al., 1984; Padisák, 1985; Heaney
et al., 1988; Rengefors et al., 1998). C. hirundinella
population success seems to decrease in these systems with increasing mixing depth (George & Heaney,
1978; Heaney & Talling, 1980; Reynolds et al., 1983)
probably as result of reduced light availability and/or
lower temperatures during the autumn mixing period.
However, most studies on C. hirundinella population
seasonality were in northern north-temperate systems
(45–60 ◦ N) and there are scant data on this issue at
lower latitudes. If light and temperature conditions restrict C. hirundinella populations to a few months in
northern north-temperate systems a different seasonal
distribution can be expected in warmer and sunnier climates. In the subtropical Lake Kinneret (32◦ 45–53’
N, Israel), for instance, C. hirundinella populations
develop during the winter–spring period (Pollingher
& Hickel, 1991), whereas in Bermejales reservoir
(37◦ N, Southern Spain) there is an autumn-winter
population (Pérez-Martínez, 1992).
We analysed data gathered by Margalef et al.
(1976) on 100 Spanish reservoirs in order to examine the temporal occurrence of C. hirundinella in this
setting and to determine the parameters that influence
it. We hypothesised that C. hirundinella in Spanish
reservoirs would show a different temporal pattern
from that of northern north-temperate and subtropical
systems.
Methods
The present study is based on the analysis of biological, physical and chemical data gathered by Margalef et al. (1976) from 100 reservoirs distributed
throughout Spain. The reservoirs selected had a wide
102
range of climatic conditions, geological basins, ages
and morphometric and hydraulic features. All the
largest Spanish reservoirs (83% of reservoirs >50
Hm3 ) were included and some smaller reservoirs (17%
of reservoirs <50 Hm3 ) were also included when they
were important for drinking water supply. Ninety two
percent of the reservoirs had more than 20 m of maximum depth. Each reservoir was sampled on four
occasions: 1972–73 autumn–winter, 1973 summer,
1974 spring and 1974–75 winter. Samples were taken
from the deepest part of the reservoir at depths of 0, 2,
5, and 20 m (or maximum depth if <20 m). A total of
22 parameters were determined in the original study:
−
temperature, O2 , pH, alkalinity, SO−
4 , SH2 , Cl ,
++
++
+
+
Ca , Mg , Na , K , Fe, Mn, SiO3 , SRP, NO−
3,
NO−
,
chlorophyll,
primary
production,
D
,
Sec430/665
2
chi disk visibility and light extinction. The following
parameters were selected for the present analysis:
temperature, alkalinity, calcium, magnesium, sulfate,
SRP, nitrate, chlorophyll and Secchi disk visibility.
The parameters selected were those that we considered
would have a greater influence on Ceratium presence/absence and on which there were data available
for all the reservoirs. The sampling and analysis methods were described by Margalef et al. (1976). Chemical analysis methods were the following: Golterman
& Clymo (1969) for alkalinity, Shinn (1941) for nitrate
concentration (after reduction by a cadmium–copper
column), Murphy & Riley (1962) for SRP, filtration by
Whatman GF/C and methanol extraction for chlorophyll, gravimetric method by barium sulfate precipitation for high sulfate concentrations and volumetric
method by barium sulfate precipitation for low sulfate
concentrations (Rodier, 1990) and atomic absorption
for calcium and magnesium. The arithmetic mean of
the four samples in the water column was used for the
statistical analyses.
Phytoplankton samples were taken with a net, immediately fixed with Lugol’s solution, and counted
following the Utermöhl’s technique. The abundance
of C. hirundinella was reported according to an arbitrary system from 0 (= no Ceratium) to 5 (= maximum
density), following a logarithmic scale (Margalef et
al., 1976).
Non-parametric tests were used for statistical analyses because of the non-normal distribution of variables and the heterogeneity of variances. To determine
the relationship of some selected parameters to C.
hirundinella occurrence, we performed a logistic regression with a maximum likelihood loss function
(Sokal & Rohlf, 1995). The Mann–Whitney U-test
was performed to analyse differences in the stratification pattern, in the concentrations of some elements
and in Secchi disk visibility values between reservoirs
with and without Ceratium presence.
Results
The study showed that C. hirundinella is a common
species in Spanish reservoirs, with 74 of the 100 in
the study containing C. hirundinella cells at some time
of the year. The species was present during all four
seasons in 70% of the Ceratium-reservoir and during
winter time in 78% of them. C. hirundinella was restricted to spring–summer time in only 22% of the 74
Ceratium-reservoirs.
Table 1 shows the range of different variables in
the reservoirs at the four sampling times. In order to
simplify the analysis, we performed a Principal Component Analysis (PCA) to group the chemical and
physical variables (Table 2). The first component accounted for 38% of the total explained variance and
significantly and positively correlated alkalinity values, SO4 − , Ca++ and Mg++ concentrations. This
component may be associated to water ionic content.
The second component did not group variables. The
factor scores of the first component were considered as
the ionic content variable for the statistical analyses.
There were significant differences in water ionic
content and nitrate and chlorophyll concentrations
between reservoirs with and without C. hirundinella
(Fig. 1) but no differences in SRP concentration or
Secchi disk visibility. In order to determine the relationship of the first three parameters to C. hirundinella
occurrence, we performed a logistic regression considering the ionic content level and the chlorophyll
and nitrate concentrations as independent variables
and the presence or absence of C. hirundinella (scored
as 0 and 1, respectively) as the dependent variable.
In the logistic regression, the dependent variable was
logistic-transformed, log [p/(1–p)], where p is the
probability of C. hirundinella occurring. This analysis showed a significant regression coefficient for the
three variables. However, the classifications of cases
(prediction of cases) and odds ratios were very high
for ionic content, whereas they were not significant for
chlorophyll and nitrate concentrations (Table 3). The
logistic regression coefficient for ionic content was
significantly >0, indicating that the probability of C.
hirundinella presence increased with increasing water
103
Table 1. Range, mean value (estimated from the water column mean value) and median value
of the analysed variables in all the reservoirs. Median value of the analysed variables in those
reservoirs with Ceratium presence (Ceratium-reservoirs)
Variable
Range
Temperature (◦ C)
Alkalinity (meq.l−1 )
Calcium (µg.l−1 )
Magnesium (µg.l−1 )
Sulfate (µg.l−1 )
SRP (µg.l−1 )
Nitrate (µg.l−1 )
Chlorophyll (µg.l−1 )
All reservoirs
Mean ± s.e.
4.10–24.80
0.01–4.32
0.00–639.75
0.05–99.99
0.00–7.28
0.00–18.69
0.00–648.84
0.18–108.83
Figure 1. Mean value and standard error of ionic content level
(factor 1 of PCA), chlorophyll and nitrate concentration of the reservoirs where C. hirundinella is absent = 0 and where C. hirundinella
is present = 1. P-level <0.001 for ionic content, nitrate and
chlorophyll concentration (Mann–Whitney U-test).
12.89±0.23
1.69±0.06
35.28±2.72
10.40±0.71
0.80±0.06
0.72±0.08
22.87±2.12
5.26±0.49
Median
Ceratium-reservoirs
Median
12.38
1.66
22.02
4.88
0.32
0.24
13.31
2.57
12.28
2.00
29.00
7.79
0.49
0.24
17.14
2.17
Figure 2. Mean and standard error of ionic content level of the
reservoirs with (=1) and without (=0) C. hirundinella winter populations (above) and with (=1) and without (=0) all-season populations
(below) within the 74 reservoirs where C. hirundinella is present.
104
Table 2. Factor loadings of the variables involved in the Principal Component Analysis. Significantly correlated variables
are marked with an asterisk
Variable
Factor 1
Factor 2
Temperature
Alkalinity
Calcium
Magnesium
Sulfate
SRP
Nitrate
–
0.727∗
0.725∗
0.865∗
–
–
–
−0.845∗
–
–
–
–
–
–
% Total explained variance
0.380
0.156
ionic content level and hence that reservoirs with high
ionic content were more likely to have C. hirundinella.
Among the 74 reservoirs with C. hirundinella occurrence, the Mann–Whitney U-test showed higher
ionic content values in the reservoirs with winter or
all-seasons C. hirundinella populations than in those
without (Fig. 2; U-test, both p< 0.001).
Fifty-two of the studied reservoirs were stratified
at summer sampling time (22 of them were also stratified at spring) while 47 of the reservoirs were not
stratified at any sampling time. Of the 182 samples
where C. hirundinella was present, 31.3% were from
stratified and 68.7% from non-stratified water. Among
the 74 Ceratium-reservoirs, the species was present
in both those with (52) and those without (22) a
stratification period, although C. hirundinella was
more frequent in the reservoirs with a stratification
period than in those without (Mann–Whitney U-test,
p<0.001). It is important to note the higher ionic content in reservoirs that stratified than in those that did
not (Mann–Whitney U-test, p<0.001).
Regarding light conditions, no differences in Secchi disk visibility were found between samples with
and without C. hirundinella presence (Mann–Whitney
U-test, p>0.05).
Discussion
The long-established characterisation of C. hirundinella as a warm and stratified water species (Hutchinson, 1967; Round, 1981; Wetzel, 1981; Margalef,
1983; Sommer et al., 1986), with populations restricted to a few months per year (Reynolds, 1984),
is challenged by our finding that C. hirundinella is
very commonly present in Spanish reservoirs in winter
time. Heaney et al. (1988) reported that low light intensity and low temperature levels probably inhibit C.
hirundinella development during autumn–winter time.
C. hirundinella limitation by these factors is unlikely
in Spain, where the light intensity values and number
of sunny days are much higher than in northern northtemperate regions. No light data are available in this
study but our data on Bermejales reservoir (Southern
Spain) indicated that growth is not limited by light
conditions (Pérez-Martínez & Sánchez-Castillo, submitted). Moreover, no differences were found in Secchi disk visibility between samples with and without
Ceratium. The range of temperature values for the
reservoirs studied was 4.10–24.8 ◦ C. Given that the
minimum temperature for C. hirundinella excystment
and appearance in temperate systems has been reported to be 4 ◦ C (Heaney et al., 1983; Rengefors et al.,
1998), this taxon could be present throughout the year
in Spanish reservoirs. Unfortunately, although cysts
were observed during the study, no data on Ceratium
cysts were available from Margalef et al. (1976).
Most of the field studies on C. hirundinella ecology have been carried out in northern north-temperate
systems, where winter conditions probably inhibit C.
hirundinella permanence. However, at southern northtemperate latitudes, the temperature and light conditions would allow the development of C. hirundinella
at any time of the year. In fact, studies of C.
hirundinella populations of subtropical Lake Kinneret
(32 ◦ N) (Pollingher & Hickel, 1991) showed the
presence of winter-spring populations. Permanent and
autumn/winter C. hirundinella populations have been
also reported in several Spanish reservoirs (Toja et
al., 1981; Araúzo-Sánchez, 1992; Pérez-Martínez,
1992; Hernández, 1997; Galindo, 1998). In addition,
Sicilian lakes and reservoirs showed autumn–winter
C. hirundinella populations in 9 of the 16 systems
where this taxon was present (Calvo et al., 1993) and
Naselli-Flores & Barone (1999) indicate that Ceratium
hirundinella is mainly present in Rosamarina reservoir in winter and early-spring, when deeper mixing
depth and higher transparency values occur. These
data suggest that winter populations of C. hirundinella
are relatively frequent in southern north-temperate
systems.
The hydraulic regime can considerably modulate
the structure of phytoplankton assemblages in lakes
(García de Emiliani, 1997; Huszar & Reynolds, 1997)
and reservoirs (Kimmel et al., 1990; Naselli-Flores,
1999). The common hydraulic regime in Spanish
105
Table 3. Results of the logistic regression between presence (= 1) or absence (= 0) of C. hirundinella as dependent variable and water
ionic content (Factor 1 of PCA), chlorophyll and nitrate concentration as independent variables. Analyses performed on the four
annual samples from each reservoir. R.C. = regression coefficient
Intercept
Ionic content
Chlorophyll
Nitrate
2.648
1.250
0.488
p-level
R.C.
p-level
<0.001 3.322
<0.001 −0.027
<0.01
0.037
<0.001
<0.05
<0.001
X2
p-level
df
n
% correct
predicted 0
150.27 <0.001
5.59 <0.001
28.81 <0.001
1
1
1
384
383
390
82.11
1.04
0.00
reservoirs consists of a decrease in water volume
during summer time, caused by a high outflow and
low inflow, and an increase in water volume during
autumn–winter, caused by a low outflow and high inflow. Naselli-Flores (1999) described drastic changes
in the structure of phytoplankton assemblages in Sicilian reservoirs subsequent to modifications in the
stratification pattern by the large summer outflow.
It is likely that the abundance and presence of C.
hirundinella during the dry season could be affected
by this factor in many Spanish reservoirs. However,
this would not affect the autumn-winter presence of
the species. On the other hand, washout (dilution rate)
has been suggested as a limiting factor for winter populations of Ceratium spp. in English lakes (Heaney et
al., 1983). The hydraulic regime of Spanish reservoirs
would not impede the development of C. hirundinella
population in winter time because washout does not
operate as it does in lakes with a stable water level.
As commented by Heaney et al. (1988), it remains to
be demonstrated whether washout plays a determinant
role in C. hirundinella growth in freshwater systems.
The water ionic content strongly predicted the occurrence of C. hirundinella in the reservoirs studied,
which is in line with the description of this taxon
as a species of alkaline waters (Hutchinson, 1967;
Pollingher, 1987; Talling, 1976). Bruno & McLaughlin (1977) also observed maximum C. hirundinella
growth in laboratory cultures at high Ca2+ and Mg2+
concentrations. The positive relationship between C.
hirundinella presence and waters of high ionic content is also shown in Margalef et al. (1976, 1982) and
in the study by Sabater & Nolla (1991) on the same
group of reservoirs during 1987–1988. Winter and/or
all-season Ceratium populations occurred more frequently in high ionic content reservoirs than in those
with low ionic content (Fig. 2). Given that the temperature and light conditions of Spanish reservoirs
permit the development of C. hirundinella in any sea-
% correct
predicted 1
91.70
98.61
100
Odds ratio
50.66
0.75
–
son, this suggests that the occurrence of winter and/or
all-season populations mainly relies on ionic content.
Our study on Bermejales reservoir (Pérez-Martínez &
Sánchez-Castillo, submitted) also showed a clear relation between C. hirundinella density and water ionic
content level. On the other hand, C. hirundinella populations are also found in low ionic content waters of
Swedish and English lakes (Nauwerck, 1963; Heaney
et al., 1988). Thus, the influence of parameters associated to ionic content on the growth of C. hirundinella
has yet to be elucidated. Another aspect to consider is
the taxonomic and genetic differences between populations. Differences in the seasonal distribution of C.
hirundinella populations between systems might be
related to presence of different Ceratium species or
even of different genetic forms (ecotypes) within species. For example, differences between the freshwater
species of Ceratium genera were barely discerned until the 1990s, with the result that C. hirundinella was
considered to be widely distributed. For instance, C.
furcoides in the English Lake District was long regarded as a form variant of C. hirundinella (Heaney et
al., 1988) and Hickel (1988) described C. rhomvoides
as a new species that coexisted with the former two
species in Lake Plußsee.
There is no clear relationship between stratification
conditions and Ceratium presence. The more frequent
presence of C. hirundinella in reservoirs that stratified
is not conclusive, because these reservoirs also showed
a higher ionic content than those that did not stratify.
Furthermore, C. hirundinella was present in both stratified and non-stratified waters and during the mixing
period in reservoirs that stratified in summer time.
In conclusion, our findings on the temporal occurrence of C. hirundinella in southern north-temperate
systems are not consistent with its characterisation as
a typical species of warm waters and stratified conditions. C. hirundinella is very common in winter
time in Spanish reservoirs, despite the mixing con-
106
ditions and lower temperatures and light availability.
The presence of the species is positively related to the
water ionic content (HCO3 − , SO4 2− , Ca2+ , Mg2+ ).
Further studies are required on C. hirundinella taxonomy and temporality along latitudinal gradients as
well as laboratory and field experiments on the factors
that determine its growth.
Acknowledgements
We thank Richard Davies for linguistic assistance with
the English. The authors are grateful to Dr Margalef
for his interest in the manuscript.
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