J. Microbiol. Biotechnol.

(2012), 22(6), 754–762

http://dx.doi.org/10.4014/jmb.1110.10005
First published online April 11, 2012
pISSN 1017-7825 eISSN 1738-8872

Dinophyceae Fluctuations in Two Alpine Lakes of Contrasting Size During

a 10-Year Fortnightly Survey
Trevisan, R.1, R. Pertile2, V. Bronamonte1, F. B. Dazzo3, and A. Squartini4*
1
Dipartimento di Biologia, Universit di Padova, Viale G. Colombo 3, 35129, Padova, Italy
2
Epidemiological Observatory of the Provincial Centre for Health Services, Viale Verona, 38100, Trento, Italy
3
Department of Microbiology and Molecular Genetics, Michigan State University, East Lansing, MI 48824, USA
4
Dipartimento di Biotecnologie Agrarie, Universit di Padova, Viale dell’Universit 16, 35020 Legnaro, Padova, Italy
Received: October 4, 2011 / Revised: January 22, 2012 / Accepted: February 6, 2012

Colbricon Superiore and Inferiore are two small adjacent
high-mountain lakes located in the Paneveggio Natural
Park (Italy) that offer the rare opportunity to study two
iso-ecologic water environments differing only by area
and volume in a ratio of 2:1 and 3:1, respectively. We took
advantage of this setting to investigate phytoplankton
dynamics, compare variability and productivity differences
between the two basins, and assess size-dependent issues.
The phytoplankton group of the Dinophyceae was chosen
as the indicator organisms of ecological perturbation owing
to their high sensitivity to environmental variations, as
well as their acknowledged nature of versatile proxy to
report global climatic changes. The study was conducted
for over 10 years with fortnightly samplings. Results
indicated that (a) the Dinophyceae communities in the
smaller lake were significantly more resistant to changes
exerted by the fluctuation of lakewater transparency and
pH; and (b) the smaller lake sustained a consistently higher
production with an average Dinophyceae density 1.73 fold
higher than that of the larger lake. The coefficients of
variation show that the chemical parameters in the
smaller lake display higher time-related fluctuation while
being spatially homogeneous and that such conditions
correlate with a higher stability of the Dinophyceae
assemblage. The use of this setting is also proposed as a
model to test relationships between ecosystem production
and physical stability.
Keywords: High-mountain lakes, Dinophyceae, environmental
variables, microbial ecology, Colbricon Lakes, Paneveggio-
Pale di S. Martino Natural Park
*Corresponding author
Phone: +39-498272923; Fax: +39-498272929;
E-mail: squart@unipd.it
Lakes occurring at high mountain altitudes are particularly
interesting habitats for ecological studies [8, 24] since they
represent small, fragile, highly individual ecosystems, like
islands of biodiversity surrounded by a sea of land [13]. In
Italy, the majority of natural lakes smaller than 0.2 km2 are
located in the Alps, and most originate by glacial modeling,
causing the formation of either basin erosion or of a morenic
barrier. The so-called “cirque lakes” are most frequent and
often grouped along an altimetric sequence [2]. Lakes at
higher altitudes are more recent, fed by melting snow and
rainfall, and have relatively shallow depths and often
fluctuating water level [27].
Harsh climatic conditions characteristically occur in
remote mountain lakes. They experience low temperatures,
short ice-free periods, and variations in precipitation
(snow) that are prone to cause pronounced seasonal
variations in water chemistry [23, 30] and changes in
biotic assemblages [15, 20]. Such ecosystems generally do
not exhibit obvious anthropic disturbances such as single-
point pollution sources or changes of land use in the
drainage area. Owing to the geological features of the
catchment areas in the mountain region, as is the case of
the acid bedrock Lagorai range, many high mountain lakes
are poorly buffered in pH and several display acidification
phenomena [4]. For these reasons, they are considered
simple and labile ecosystems that react promptly to
environmental changes and stresses. Because of this sensitivity,
high mountain lakes can function as early warning systems
for environmental changes related to climate and other
factors, thus providing information that goes beyond the
interest in their intrinsic ecosystem structure [30]. They
offer ideal systems to monitor the effect of global climate
changes through the analyses of their phytoplankton
dynamics [40, 41]. Analyses of the biotic components and
their fluctuations can therefore provide insights on global
755 Trevisan et al.
phenomena and facilitate their predictions for either
management or conservation purposes.
Knowledge of algal communities in high mountain
lakes indicates that, rather than supporting endemic or
specialized taxa, these environments display a rarefaction
on the general checklist found in larger lakes at lower
altitudes [9, 29]. In addition, the process of selection of the
species able to persist in these alpine environments is
determined by their ability to survive the alternating
phases of short vegetative periods and ice-covered stages,
with adaptation to opposite light regimes, from the intense
summer radiation to the weak ice-filtered shady winter
situation. Phytoplanktonic species in these situations need
also to endure low nutrient availability and fluctuating
water regimes due to atmospheric precipitations and
freezing/thawing cycles [39]. Traits of adaptation include
their small size dimension [47] and active dispersal
capabilities mediated by their flagellated motility [32, 36].
Low phytoplankton biovolumes generally occur in these
lakes with the possibility of summer or fall seasonal peaks
[9, 22, 29]. Peaking can also be due to nutrient increase or
interactions with other members of the community. Studies
have also been devoted to analyze the effects of global
climate change on these communities [6, 11, 18].
Among freshwater eukaryotic microorganisms, dinophyceae
are particularly suitable proxies for climate changes, allowing
to extrapolate universally valid patterns [45]. Their features
of usefulness are abundance, autonomous movement
capabilities, adaptation to oligotrophy, possibility of cyst
formation, and permanence in sediments (providing records
for analyses of past events). This group of microbial
eukaryotic algae can be abundant both in marine and
freshwater environments. Over 2,000 species have been
described, and only half of these are photosynthetic [46].
The group includes autotrophs, mixotrophs, and fully
heterotrophic phagotrophs. They show remarkable biochemical
diversity, varying in the composition of photosynthetic
pigments and ability to produce toxins. Many of the
photosynthetic ones are mixotrophs, and the heterotrophs
can feed upon bacterioplankton using a wide variety of
mechanisms [16, 42]. Among the freshwater planktonic
species, few dinoflagellates have been described after
Bourrelly’s monograph [5] reporting 220 taxa. Moreover,
the extant ones are defined as “morphospecies,” in the
classical sense. The suitable species concept to be applied
to dinoflagellates or other harmful species has been
discussed [25]. Freshwater dinoflagellates efficiently migrate
vertically along the water column, usually displaying
chemotaxis downwards at night to pursue nutrients and
phototaxis upwards to the photic zone at daytime for
photosynthetic purposes [43]. Different ecological studies
on phytoplankton phyla in high mountain lakes have found
common trends and shaping factors [9, 22]. Hansen and
Flaim [19] surveyed the occurrence of dinoflagellates in 27
lakes of the Trentino region in Italy, and reported the
presence of 34 taxa.
In the present study, we took advantage of the rare
opportunity offered by the two adjacent lakes of Colbricon
as a consequence of their geomorphological situation.
Located next to each other, the smaller lake (Colbricon
Inferiore, C.I.) has one-third the volume of the larger lake
(Colbricon Superiore, C.S.), allowing an interesting configuration
to investigate size-related effects in waterbodies within the
same landscape and under equal geochemical influxes.
Such availability of two lakes differing by size and depth
has been envisaged as a particularly useful setting to
compare stability and productivity in relation to possible
differences in homogeneity of their physical and chemical
profiles. The study presented here extends over a particularly
wide temporal window (10 consecutive years), throughout
which the lakes were sampled with consistent intensity
(about fortnightly in the ice-free periods), providing an
uncommonly large dataset compared with most standards
of phytoplankton studies.
MATERIALS AND METHODS
The Site
We analyzed Colbricon Superiore (C.S., 1,922 m a.s.l.) and Colbricon
Inferiore (C. I., 1,910 m a.s.l.), which are two alpine lakes located in
the Lagorai mountain range within the Avisio basin, located in the
Paneveggio-Pale di S. Martino Natural Park (Trento, Italy) (maps in
Fig. 1). Lake C.S. features a surface nearly twice the area of Lake
C.I. and a volume about three times larger. The area of Lake C.S. is
0.024 km2 and its volume is 0.13 km3, whereas the same values for
Lake C.I. are 0.013 km2 and 0.05 km3, respectively. Their close
proximity (the lakes are separated by less than 50 m) and the
consequent sharing of the same water catchment basin constitute a
set of features allowing to perform size-dependent comparisons
independent of other environmental variables. The lakes lie on peat
soil overlying a bedrock substratum of quartziferous porphyry, and
are surrounded by a sphagnum and sedge vegetation [14]. As glacial
cirque lakes, they are small and relatively shallow, with maximum
depths of 12 m and 8 m and average depths of 5.4 m and 3.8 m,
respectively. They are dimictic, undergoing complete mixing in
spring and autumn, and their morphological and hydrological features
have been previously described [49].
Field Methods and Laboratory Analyses
Both lakes were monitored and sampled over a decade. As these
lakes generally freeze from November to May, the sampling scheme
represented the 10 ice-free periods between years 1998 and 2007,
corresponding to a sampling interval of every 2 or 3 weeks. The
analysis schedule involved on average 7 sampling dates each year,
yielding a total of 69 samplings per lake. Hydrometric level, air and
water temperature, transparency, pH, and conductivity were measured
in situ, and chemical analyses of water samples (depth-integrated
across the water column) were performed at the Institute for the
Study of Ecosystems CNR-ISE of Verbania-Pallanza according to
standard methods [44]. Water level was measured by a fixed
 DINOPHYCEAE AND ENVIRONMENTAL VARIABILITY IN ALPINE LAKES 756

Table 1. Ranges of the main physical and chemical water

parameters of Colbricon Lakes during the 10 years of study, from
1998 to 2007.
L. Colbricon L. Colbricon
Superiore Inferiore
Mean Min Max Mean Min Max
o
Mean water T C 11.2 2.0 18.0 11.3 2.0 18.0
Water level (cm)a 101 93 115 90 76 111
Transparency (m) 5.0 1.1 8.4 4.15 1.2 7.0
pH 7.3 6.9 7.6 7.4 6.9 8.2
o
χ20 C
45.77 40.00 49.90 44.17 37.60 55.00
µS/cm
Total alkalinity
0.44 0.37 0.49 0.44 0.34 0.67
meq/l
Cl
0.41 0.28 0.75 0.40 0.27 0.71
mg/l
SO4
1.64 1.37 1.62 1.53 1.13 1.99
mg/l
Ca
8.53 7.15 9.86 8.49 6.30 12.70
mg/l
Mg
0.31 0.27 0.33 0.28 0.22 0.46
mg/l
Na
0.80 0.70 0.95 0.84 0.71 1.04
mg/l
K
0.32 0.11 0.50 0.23 0.16 0.58
mg/l
N-NO3
135 44 204 149 5 268
Fig. 1. Maps of the study area. µg/l
(a) Indication of the site location (*) in Italy; (b) local map of the area N-NH4
83 28 140 68 12 213
showing the 2 neighboring lakes (shaded) examined in this study; (c, d) µg/l
batimetric maps (in m) in the Lakes Colbricon Superiore (c) and Colbricon Total N
Inferiore (d). Scale bars represent 200 m in b and 50 m in c and d. 440 310 630 470 280 870
µg/l
Reactive P
2 1 5 5 2 18
µg/l
graduated stick set at 100 = 1,922 m a.s.l. (C.S.) and 0 = 1,910 m Total P
a.s.l. (C.I.). Trophic classification of the lakes was defined using 12 4 37 14 3 47
µg/l
indexes based on Secchi disk transparency and total phosphorus Si
concentration, according to Hakanson [17] and to the OECD model 0.94 0.60 1.42 1.32 0.91 1.79
mg/l
[26]. Integrated samples from the whole water column for the
a
quantitative analysis of phytoplankton density and biomass were The water level measurement is relative to a graduated stick set at 100 =
taken by a plastic flexible hosepipe siphon tube [49, 51]. In parallel, 1,922 m a.s.l. (Lake C.S.) and 100 = 1,910 m a.s.l. (Lake C.I.).
water samples for additional (qualitative only) taxonomic analyses
were collected with a 25 µm plankton net, upon rowing for 15 min software (SPSS Inc., Chicago, IL, USA), using as outcome variables
across the main lake axis. the Dinophyceae density and biomass in each of the two lakes.
Samples were fixed with Lugol’s solution and were examined by Ecological indices, relative to the community diversity (Brillouin
brightfield light microscopy using an inverted microscope at 400× Diversity Index), and pairwise dissimilarity coefficients (Bray-Curtis
magnification, in accordance with the Utermohl technique [50], and and Chord distances) were computed using an in-house Center for
by SEM [19] for some specific identifications. The keys of Popovsky Microbial Ecology Image Analysis System (CMEIAS) data analysis
and Pfiester [33, 34] and Hansen and Flaim [19] were used for addin [12] operating within Excel.
taxonomic determination. Sample biomass was estimated by
multiplying known reference biovolumes [38] for the different taxa
identified. Relative Water Column Stability (RWCS) was calculated RESULTS
as described previously [31].
In order to examine the causally connected correlations between
The mean water temperatures and temperature ranges
variations in algal fluctuations and environmental parameters, a
multivariate Poisson regression analysis was performed by SPSS
during the whole study period were closely similar in the
757 Trevisan et al.

Table 2. List of the Dinophyceae taxa observed in the two lakes and their mean density and biomass throughout the 10 years.
Colbricon Superiore Colbricon Inferiore
Mean density Mean biomass Mean density Mean biomass
Taxon Occurrence Occurrence
(cells/ml) (mg/m3) (cells/ml) (mg/m3)
Peridinium goslaviense 9.7 43 97.53 25.0 48 250.45
Peridinium spp. 8.8 40 133.08 9.0 35 135.72
Gymnodinium sp. 3.6 20 54.04 4.5 28 67.62
Peridinium volzii 1.1 12 16.38 2.0 10 30.36
Ceratium hirundinella 0.09 1 1.78 0.41 5 8.30
The occurrence columns indicate the frequency of presence; that is, in how many of the 69 samplings a given taxon was found.

two lakes (Table 1). However, during the same 10 year
period, the Relative Water Column Stratification Stability
index (RWCS) [31] had an average value of 50.34 for Lake
C.S. and a significantly lower value of 36.55 for Lake C.I.
Both lakes had average pH values that were close to
neutrality (7.3-7.4) and low mean conductivity (~ 45 µS/cm),
consistent with a limited salinity condition. The mean ratio
of total nitrogen (TN) to total phosphorus concentrations
was 36.6 in the C.S. and 33.5 in the C.I. Since this ratio
exceeds a value of 10, total phosphorus is likely to be
the limiting growth factor for phytoplankton [10]. The
concentration of reactive phosphorus was the only parameter
that had a noteworthy difference between the two lakes.
The amounts recorded were 2 µg/l (C.S.) vs. 5 µg/l (C.I.).
Mean reactive soluble silica concentrations were also
slightly higher in the smaller lake. During the study period,
both lakes would be categorized as mesotrophic based on
their transparency values and total phosphorus concentrations
[16, 26].
The microscopical examinations of the 138 integrated
samples collected in both Colbricon Lakes during the 10
year study (quantitative analysis) allowed species identification
(Table 2). Five taxa of Dinophyceae were found, including
Peridinium volzii Lemmermann, Peridinium goslaviense
Woloszynska; Peridinium sp. Ehrenberg, Gymnodinium
sp. Stein, and Ceratium hirundinella (O.F. Müller)
Dujardin. In Lake C.S. the 10-year average cell density of
the Dinophyceae was 23.7 cells/ml. In the lower Lake C.I.,
their cell density was 41.0 cells/ml. Regarding the
corresponding cumulative biomass values (estimated by
multiplying the cell density of each taxon by its unit
volume reported in the literature), the mean was 302.8 mg/m3
in Lake C.S. and 492.4 mg/m3 in Lake C.I.
Fig. 2 shows the mean cell densities of the five different
taxonomical entities of Dinophyceae found in these lakes.
The dominant density of the Peridiniaceae is responsible
for the nearly 2-fold higher Dinophyceae abundance in the
lower lake as compared with the upper one. On the
contrary, Gymnodinium and Ceratium genera are approximately
equally abundant in both lakes.
The differences in relative distribution of abundance
among these dinoflagellate species were evaluated based
on their relative proportions of individuals present and
their cumulative biomass. The ordinal Brillouin index was
chosen for comparisons of their diversity and evenness
because of its low sensitivity to variation in sample size,
sensitivity to abundance of rare species, and usefulness
when non-random collections are being estimated. The
percentage dissimilarity, and Bray-Curtis and Chord
distance coefficients all indicated that the difference in
distributions of abundance among these 5 dinoflagellate
species within the 2 lakes was greater when based on
relative proportions of their cumulative biomass rather
than their individual counts (Table 3).

Table 3. Differences in relative distribution of abundance among

dinoflagellate species measured by distance dissimilarity coefficients.
Distance based on proportions of:
Dissimilarity coefficient Individuals Cumulative
Fig. 2. Mean 10-year densities (cells/ml) of the main Dinophyceae present biomass
taxa in Lake Colbricon Superiore (C. S.) and Lake Colbricon % Dissimilarity 9.10 20.26
Inferiore (C. I.). Bray-Curtis distance 0.091 0.203
C. h: Ceratium hirundinella; G. sp.; Gymnodinium sp.; P.v.: Peridinium
volzii; P. g.: Peridinium goslaviense; P. sp. : Peridinium sp. Chord distance 0.170 0.425
 DINOPHYCEAE AND ENVIRONMENTAL VARIABILITY IN ALPINE LAKES 758

Fig. 3. Biomass values (mg/m, Y-axis) of the Dinophyceae in the two lakes throughout the 10-year sampling period.
White bars: Lake Colbricon Superiore; black bars: Lake Colbricon Inferiore.

Fig. 3 shows the date-by-date abundance of the Dinophyceae
biomass throughout the whole 10-year study. Large
fluctuations occurred and, with the exception of some
seasonal occurrences, the lower lake supported a higher
biomass of Dinophyceae. The biomass of Dinophyceae
(mg/m) was higher in the smaller C.I. lake than in the
larger C.S. lake in 50 of the 69 samples.
In order to test for correlations between chemical or
physical parameters and biological counts, the data
distribution was first verified using the Poisson model.
This type of analysis was chosen because the dependent
variables were not normally distributed and the distribution
was right-skewed with one tail on the right having the
following skew values: density C.S. and density C.I.:
skew = 1.72; biomass C.S.: skew =1.57; biomass C.I.:
skew = 1.45. A multivariate Poisson regression analysis
was accordingly run and highlighted some significant
instances. The interpretation of Poisson regression was
presented in terms of incidence rate ratios (IRR). For each
continuous variable, the estimated rate ratio for the
dependent variable is expressed for a one unit increase in
the independent one, with the other variables being held
constant in the model.
As Table 4 shows, the most noticeable feature is a
negative correlation with water transparency. This occurred
in both lakes and was more severe in the superior one

Table 4. Poisson regression analysis using as outcome variable density and biomass of the Dinophyceae in the Colbricon Superiore and
Inferiore lakes.
Lake Colbricon Superiore Density Biomass
Covariates IRR* p-Value 95% Conf.Interval** IRR* p-value 95% Conf.Interval**
Mean water temperature 1.08 < 0.0001 104-112 1.06 < 0.0001 1.05-1.07
pH 1.13 < 0.0001 1.07-1.19 1.14 < 0.0001 1.13-1.16
Conductivity 0.94 < 0.0001 0.93-0.95 0.93 < 0.0001 0.93-0.94
Transparency 0.74 < 0.0001 0.71-0.77 0.76 < 0.0001 0.75-0.76
Water level 1.01 0.001 1.00-1.01 1.01 < 0.0001 1.01-1.01
Rainfall 0.99 < 0.0001 0.99-0.99 0.99 < 0.0001 0.99-0.99
RWCS 0.99 < 0.0001 0.99-0.99 0.99 < 0.0001 0.99-0.99
Pseudo R2 ***= 0.3654 Pseudo R2 ***= 0.4394
Lake Colbricon Inferiore Density Biomass
Mean water temperature 0.98 0.484 0.93-1.04 0.97 < 0.0001 0.95-0.98
pH 1.00 0.832 0.96-1.05 1.00 0.664 0.98-1.01
Conductivity 1.00 0.420 0.99-1.01 0.99 < 0.0001 0.99-0.99
Transparency 0.87 < 0.0001 0.83-0.90 0.84 < 0.0001 0.83-0.85
Water level 0.98 < 0.0001 0.98-0.99 0.99 < 0.0001 0.98-0.99
Rainfall 1.00 0.146 1.00-1.00 1.00 0.184 1.00-1.00
RWCS 1.00 < 0.0001 0.99-1.00 0.99 < 0.0001 0.99-0.99
Pseudo R2 ***= 0.1934 Pseudo R2 ***= 0.2256
*IRR: Incidence Rate Ratios for the Poisson model, obtained by exponentiating the Poisson regression coefficient. In boldface: significant p-values and
IRRs of variables displaying variations >5%.
**95% Conf. Interval: Confidence interval for the rate ratio, given the other predictors are in the model.
***McFadden’s Pseudo R2, given by the formula (1 - L1/L0), where L0 and L1 are the constant-only and full model log likelihoods, respectively.
759 Trevisan et al.
where the IRR values for cell density and biomass are 0.74
and 0.76, representing about a 25% decrease in Dinophyceae
per unit increase of transparency. Interestingly, the
relationship was less pronounced in the adjacent smaller
lake, causing a decrease around 15% (IRR = 0.87 for
density, 0.84 for biomass). Another parameter that had a
significant negative relationship to algal dynamics was the
conductivity in the superior lake. In addition, positive
noteworthy correlations were displayed by pH in Lake C.I.
DISCUSSION
The chemical values displayed by Colbricon Superiore and
Inferiore Lakes show common features, consistent with the
fact that they belong to the same hydrological basin and
are connected by a short effluent running from C.S. Since
the substratum is based on non-alkaline quartziferous rocks
that are not conducive to buffering dissolved carbonates,
the observed pH values likely indicate the absence of acid
rain phenomena [49]. The threshold alkalinity defining
sensitive lakes is 0.2 meq l-1 [7], and the two lakes under
consideration fall well above such threshold.
Nitrogen and phosphorus concentrations agree with
the trophic classification [16, 26]. Relatively low silica
concentrations were present as expected for high mountain
conditions, where low temperature limits SiO2 dissolution
rates and substantial precipitation as rain or snow can
cause very high flushing rates of water through the lakes.
The silica values are however regarded as non-limiting,
being well above the minimum thresholds of 0.03-
0.06 mg Si/l typically needed to support the productivity of
siliceous phytoplankton [52]. Available data on chlorophyll
a concentration of these lakes [21] average 10.68 µg/l and
support their placement in oligo- to mesotrophic water
bodies.
In terms of functional grouping [35, 36], the prevailing
presences are taxa classified in groups LO (summer
epilimnia in mesotrophic lakes) and LM (summer epilimnia
in eutrophic lakes), tolerant of low or segregated nutrients
and sensitive to mixing and to poor light intensity. These
conditions are typical of the Avisio basin lakes, and agree
with the water chemical values recorded there [48]. The
dominant taxon Peridinium goslaviense is listed in the
indicators of nutrient-rich lakes [53]. Peridinium volzii and
Ceratium hirundinella are reported among indicators of
mesotrophic-eutrophic conditions [37].
In both the lakes, the biomass values of Dinophyceae
populations (Fig. 3) were relatively low during the first 2
years of this survey, and rose from year 2000 onwards. In
both lakes, notwithstanding the difference in the biomass
attained, the fluctuations of Dinophyceae populations were
typically parallel, and only in a few instances were their
trends opposite, leading to the rise in one lake and a
decrease in the other.
As regards the relationships between biota and physico-
chemical variables, one negative correlation was with
water conductivity, which interestingly only occurred in
the larger and deeper C.S. lake.
Water transparency had a highly significant negative
correlation with both density and biomass in both lakes.
The effect was more severe for the upper lake, in that, as
the Poisson regression shows for C.S., every unit increase
in transparency causes about 25% reduction (IRR* value =
0.76), whereas in Lake C.I. such reduction is limited to about
15% (IRR* value = 0.84). In these systems, the reduced
transparency is not only considered as a possible cause but
also as a direct effect of planktonic algal growth, which
explains its negative relationship with their cell densities.
The Relative Water Column Stability (RWCS), reporting
how stable is the stratification of the temperatures in the
water column, is a parameter that has been applied in
different instances on various lakes [3, 28]. Our measurements
displayed average values of 50.34 for Lake C.S. and 36.55
for Lake C.I. (Table 2). The lower value for the smaller
lake indicates conditions more prone to mixing of the
waters, supposedly due to its shallower nature (average
depth 3.8 m) in which the wind-driven mixing involves a
more substantial portion of the lake volume compared with
the deeper C.S. lake. The more severe reduction exerted in
the deeper C.S. lake (Poisson’s IRR* = 0.76) is consistent
with the fact that such lake maintains a more stable thermal
stratification, with the consequence that light-related effects
are more effective on development of algal populations.
These data strengthen the view of a tighter control/
response of biota in the smaller lake in spite of possible
chemical and physical shifts. In the shallower lake, the
volume being one third that of the larger lake appears to
play a significant role in the dynamics of the phytoplankton,
despite the equal exposure of both neighboring lakes to
inputs from the common catchment basin. The Dynophyceae
in Lake C.I. appear to be less affected by most of the
independent variables than do their companion populations
in Lake C.S. Such resistance can be summarized as
follows: no effect by pH (vs. a 14% increase per pH unit in
Lake C.S.); no effect by conductivity (vs. a 6-7% decrease
per unit dependency in Lake C.S.), and less severe effect
by transparency (only 14% decrease per unit increase vs. a
25% decrease in Lake C.S.). This higher stability of the
Dinophyceae populations in the smaller lake where they
attain higher diversity and evenness, as well as higher
biomass and density, supports possible links between
ecosystem diversity, stability, and productivity, implementing
one of the main tenets in ecological theory.
It is worth noticing that smaller waterbodies, because of
their lower mass, are more prone to mixing and ultimately

Table 5. Evaluation of the parameter stabilities in the two lakes.
Coefficient of variation
a
Lake Chemical parameters
Colbricon Superiore 0.37
Colbricon Inferiore 0.49
Coefficients of variation for the two lakes, obtained from the means and standard deviations of the pooled chemical, physical, and biological data, calculated
over the whole decadea. Mean of the coefficients of variation of the concentrations of Cl-, SO4-2, N-NO3-, N-NH4+, Ca+2, Mg+2, K+, reactive P, total P, total N,
organic N, and organic Pb; mean of the coefficient of variation of water temperature, transparency, pH, conductivity, water level, and RWCS; cmean of the
coefficient of variation of the population density values of Dinophyceae.
to homogenization of physical and chemical profiles, and they
are at the same time exposed to higher extents of parameter
fluctuations in time, leading to more frequent disturbance
events whose effect may also positively affect diversity.
Lake C.I. was less stratified and more homogenized (lower
RWCS), being more exposed to changes of the independent
variables. Nevertheless, the Poisson regression indicated
that its Dinophyceae assemblage composition appears to
be less dependent on the variation of such environmental
variables despite their broader extent of fluctuation compared
with the deeper Lake C.S.
In order to put in evidence the extent of variation in the
physical, chemical, and biological parameters in the two
lakes during the period of study, we compared the
dispersion of the data by calculating the coefficient of
variation (standard deviation/mean) for each measured
variable using the dataset of the whole period. The values
for each of the three kinds of parameters (physical, chemical,
and biological) were then averaged. The resultant Table 5
shows that the two lakes had identical coefficients of
variation in the physical parameters, but the smaller C.I.
lake fluctuated more in chemical parameters while
simultaneously being more stable in Dinophyceae densities
than the larger C. S. lake.
To generalize the concept of these differences, a larger
lake would tend to be more homogeneous timewise
(hydrochemical constancy) but more heterogeneous spacewise
(stratification), whereas a smaller lake would be more
spacewise homogeneous (forced to mixing) and timewise
heterogeneous (displaying frequent changes in short time
frames). Within such scenarios, it appears that the biological
assemblage of the Dinophyceae better endures and
counteracts the changes when it resides in lakes that exhibit
the second type of situation.
Lake C.I is also more productive as its mean Dinophyceae
biomass is 1.6-fold higher than in Lake C.S. These data
support the view of stability and productivity as positively
correlated dimensions in freshwater ecosystems [1]. However,
it needs to be emphasized that this stability is pertaining to
the Dinophyceae community and not to the habitat parameters
per se.
The ecological indices of dominance, evenness, and
diversity in community structure were slightly different
DINOPHYCEAE AND ENVIRONMENTAL VARIABILITY IN ALPINE LAKES 760
Physical parametersb Dinophyceae densitiesc
0.34 1.17 (St. Dev.: 27,89; Mean: 23.75)
0.34 1.04 (St. Dev.: 42.95; Mean: 41.04)
between the 2 lakes when using the number of presences
recorded for the given taxa or their biovolume abundance.
However, when the two dinoflagellate communities were
compared with each other using biovolume-weighted
abundance, the levels of dissimilarity and distance between
C.S. and C.I. reveal 2- to 4-fold higher divergences than
when based on taxa presences. The evidence further
emphasizes that the dinoflagellate diversities between the
two lakes differ from each other primarily because of their
biomass-weighted distribution of species abundances rather
than their species richness.
The chemical environment of the smaller lake appears
to selectively enhance the relative abundance of different
phytoplankton members in spite of species richness
remaining constant. It can be also observed that the higher
production of the lower lake is mostly due to the species
Peridinium goslaviense and P. volzii. Different possible
reasons for the different production levels can be
hypothesized. Dissolved nutrient comparisons indicate that
the main difference between the lakes is their reactive
phosphorus content, with the lower lake having a mean
that was nearly double (mean 4.71 vs. 2.43 µg/l) and
maximum that was even larger (18 vs. 5 µg/l). However,
reactive phosphorus values were near the lower detection
limit on some sampling dates. Total P and N are instead
rather similar. A possible explanation could be linked to
their different depths. However, as both lakes are rather
shallow, the euphotic zone is in both cases extended to
their entire depth. Therefore, the hypothesis that a deeper
aphotic zone would dilute out the phytoplankton yield
leading to lower values in Lake C.S. does not seem to be a
basis to explain the observed phenomenon. A more
plausible explanation could be linked to the fact that in
front of an equal runoff of nutrient from the slopes of the
shared catchment basin, Lake C.I would be ending up with
more concentrated nutrients as these dissolve in a smaller
reservoir. Such enrichment could translate to a more
sustained biological production.
All things considered, the two neighboring Lakes of
Colbricon constitute a unique set of coupled model
environments offering the rare opportunity to study variations
imposed by some environmental constraints while keeping
other environmental variables constant. Such reduction in
761 Trevisan et al.
dimensionality involving the effect of habitat size in
homeostatic resistance is a valuable asset to address
questions of broad interest in general ecology. The
availability of a continuous dataset accumulated over 10
consecutive years is a further element of strength of the
comparison. Related studies are in progress to expand the
data to include whole community analyses that include all
the remaining phytoplankton divisions as well as the
bacterial components, in order to trace a general picture of
size-dependent responses in high mountain lake ecology.
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