Download The effect of water column mixing on phytoplankton succession

Journal of Plankton Research Vol.20 no.10 pp.1927-1951, 1998
The effect of water column mixing on phytoplankton succession,
diversity and similarity
Karl-Erich Lindenschmidt and Ingrid Chorus1
FG Siedlungswasserwirtschaft, Technische Universitat Berlin, Strafie des 17 Juni
135 (Sekr. KF 7), 10623 Berlin and' Umweltbundesamt V2.2, Postfach 33 0013,
14191 Berlin, Germany
Abstract. The lake number was used to describe the mixing condition for three consecutive years
(1992-1994) in Lake Tegel, Berlin, and compared to the successions of diatoms, dinoflagellates and
cyanobacteria, the main phytoplankton groups in the lake, as well as to diversity and similarity indices.
Using both diversity and similarity indices in juxtaposition provides an indication of the growth type
of prevailing species (r- or K-strategists) and the degree of competition in the aqua-ecological system.
A genera] pattern of these indices can be recognized as three phases: (i) high diversity—during spring,
summer and autumn, interrupted by (ii) phases of low diversity during the late spring clear-water
phase as the number of spring species plummeted, and (iii) during the late summer, climax populations of K-strategists. On a smaller time scale, similarity and diversity proved to react sensitively to
disturbances at frequencies intermediate in relation to the generation times of the phytoplankton.
This supports the 'intermediate disturbance hypothesis', as proposed for phytoplankton by Padisak
et al. [(eds) Intermediate Disturbance Hypothesis in Phytoplankton Ecology. Kluwer Academic, 1993].
Diversity may remain quite high even for extended periods during summer climax situations, in
conjunction with a high degree of similarity, if deeper mixing of the epilimnion occurs at time intervals
of 2-3 weeks, as during the summer of 1993. This enables the prevalence of 'ruderal' species, together
with some motile K-strategists who actively seek optimal depths for photosynthesis. During such
summer situations described by frequent occurrences of lower lake numbers, the epilimnion of Lake
Tegel is mixed deeply enough to support ruderals, but not too vigorously to counteract competitive
advantages of motile species. Thus, vertical niche separation enhances diversity.
Introduction
Intermediate disturbance hypothesis and water column mixing
The intermediate disturbance hypothesis (IDH) (Connell, 1978; Padisdk et al.,
1993) states that the frequency of disturbances from external forces has an effect
on the diversity of a biotic community. When the frequency (or intensity) of these
disturbances is high in comparison to the generation times of the organisms
(Figure 1), the environment is more suited for r-strategists (sensu Sommer, 1981)
since they can establish populations rapidly between disruptions. These organisms are generally fairly small, have high specific growth rates and suffer a high
mortality rate. If these perturbations occur at very low frequencies, K-strategists
(organisms optimized for low loss rates) prevail since the system remains constant
for a period of time long enough for climax populations to develop. These organisms are generally fairly large, compete very well for resources, allowing them to
displace inferior competitors and have low loss rates. In both cases, the diversity
remains low. Hence, frequent disturbances make it difficult for many species to
thrive; infrequent disturbances allow competition to reduce diversity. When
disturbances lie in an intermediate range between the two extremes of very low
and very high frequency, the diversity is increased since both r- and K-strategists
are still competing and have not reached the point of competitive exclusion. The
© Oxford University Press
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K.-E.Lindenschmidt and I.Chorus
R-S
C-R
(Strategist sensu Reynolds 1988)
mixed r and K :
(Strategist sensu Sommer 1981)
diversity
Time after disturbance
High
Magnitude of disturbance
Low
o
r - growth rate
K - carrying capacity
I
"3
Time after disturbance
High
Magnitude of disturbance
Low
Fig. L The behavior of species diversity and similarity with respect to population growth dynamics.
trade-off is the lower biomasses of each since the conditions are not at the
optimum for either strategist.
Reynolds (1997) further differentiated this concept by adding a third category
of phytoplankton growth types: the ruderals (R). These are 'attuning' or 'acclimating' strategists especially tolerant to physical perturbations, or even require turbulence to remain in suspension. They achieve relatively high growth rates even at
low or variable light intensities, and their morphology (frequently elongated or
trichal) provides a high surface/volume ratio, thus enabling rapid exchange of
metabolites through the cell surface. Analogous to r- and K-strategists, Reynolds
(1997) uses the terms competitors (C) and stress-tolerant (S) species, respectively.
The former are 'invasive' strategists characterized by small cell size, rapid nutrient absorption, assimilation and replication, and appear in the water column after
hydrological conditions have changed drastically (e.g. the onset of thermal stratification); the latter 'acquisitive' strategists are typically large cells or form colonies,
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Effect of water column mixing on phytoplankton
grow relatively slowly and are capable of buoyancy regulation to counteract turbulent conditions.
It has been stated that it is not the intensity of turbulent mixing, but rather the
depth of the mixed layer, that determines the algal loss due to sinking (Reynolds,
1989; Howarth et al., 1993). Since the highest sinking velocities are much lower
than the turbulent friction velocities generated by a wind of 1 m s"1, even the slightest wind will allow circulation of the algae in the mixed layer (Reynolds, 1989).
The bottom of the mixed layer forms a boundary layer where turbulent velocity
decreases and non-motile algae disentrain from the mixed layer into the
hypolimnion. The shallower the mixed layer, the more the algae come in contact
with this boundary layer and the greater is the loss due to sinking. On the other
hand, phytoplankton species with a higher specific density, such as diatoms, sink
more rapidly and require higher mixing intensities in order to remain suspended
in the water column (Harris, 1986). Generally, sinking rates are shown to correlate well with vertical mixing rates (Denman and Gargett, 1983). Hence, both
external forces and the strength of the water column stratification structured by
meteorological forcing must be considered to understand species composition: the
former influences the magnitude of mixing of the algae and the latter influences
the depth of this mixing. This must be combined with the frequency and duration
of the turbulent and stability events to determine the outcome of algal succession.
Bulk parameterization of water column mixing and stability
This paper investigates the possibility of using a parameter representing a bulk
summation of the various factors contributing to the stratification and mixing of
a lake as a measure for physical forcing on phytoplankton communities. The
Brunt-Vaisala frequency is often used for comparative studies of lake stability
and phytoplankton composition (Cobelas and Garcia-Moreto, 1990; Nixdorf,
1994; Rojo and Cobelas, 1994). However, only the vertical density gradient of the
water column is incorporated into the calculation and not the external forcing due
to wind. A non-dimensional parameter that incorporates these forces is the lake
number (Imberger and Patterson, 1990). This has been used as a mixing indicator
to estimate changes in dissolved oxygen (Robertson and Imberger, 1994) and
comparative studies of phytoplankton succession (Lindenschmidt and Chorus,
1997). The lake number will be used in this study to describe the mixing
conditions in Lake Tegel and as an indicative measure of intermediate disturbances on its phytoplankton.
Indices to describe ecological state
Disturbances of population development are quantified using indices of similarity
between successive sampling dates and of diversity as expressed by the Shannon
index. Possibilities of using this diversity index to investigate the applicability of
the intermediate disturbance hypothesis to phytoplankton populations were
explored at a workshop in Hungary in 1991 (Padisak et al., 1993). Whilst this
clearly showed that changes in physical conditions at a rate similar to the growth
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K.-E.Lmdenschmidt and LChorns
rate of phytoplankton populations do maintain high diversity, it also revealed that
the diversity index does not always adequately reflect the effect of perturbations—even if effects on species composition were evident. For example, a strong
mixing event can reverse the relative shares of species adapted to mixing and
species adapted to quiescence, yet the outcome of calculation of the diversity
index can be the same. To quantify the amount of change induced by a disturbance, an index is needed which compares phytoplankton associations before and
after that event. This paper introduces the application of a similarity index for
this purpose and is used as a retrospective measure of how resilient the
community proved to be.
As a testable hypothesis, it is interesting to consider both the diversity and
similarity in juxtaposition (Figure 1) to determine the nature of the ecological
environment (recently disturbed <-» equilibrium) and the stage of community
development (r-strategy <-» K-strategy). Since frequency is inversely proportional
to time, the time after a disturbance can be plotted on the x-axis, however
ascending in the opposite direction to frequency. This allows community diversity and similarity to be compared with respect to time. Immediately after a
disturbance in the environment, the similarity of the species composition with
respect to the composition prior to the disturbance will be very low. Only a few
species will have survived the disturbance and the diversity of the community will
also be low. With the migration of species into the new environment, the diversity is expected to increase. Initially, the majority of these species will be of the
r-type with high growth rates utilizing the large pool of resources made available
by the disturbance. Similarity will increase slowly as some species begin to establish themselves. As resources diminish and become limiting, species are gradually replaced by more competitive K-type species. Species diversity in this mixed
environment of both r- and K-strategists will be at its maximum. The ecological
system approaches an equilibrium point where competition by persistent and
dominating K-species causes exclusion of the less competitive species. This is
accompanied by a decrease in diversity within a phytoplankton community and
an increase in the similarity between successive sampling occasions. The position
of a community along this axis will further be influenced by the magnitude of the
disturbance: a slight disturbance will set it back only somewhat, but not all the
way to the beginning.
Using the example of Lake Tegel, this paper aims at investigating how external,
physical forces and their time scales affect phytoplankton species composition.
Further, it will test the value of using the lake number as a tool for quantifying
stability versus mixing, and thus as a measure for disturbance, and the value of
using the similarity index as a measure for the reaction of the phytoplankton
community.
Method
Description of the study site
Lake Tegel (Figure 2) is a small lake situated in Berlin, Germany, with a surface
area of 4 km2, a maximum depth of 16 m and a mean depth of 6.6 m. It is a vital
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Effect of water column mixing on phytoplankton
DEEPEST POINT (16 m)
A . METEOROLOGICAL
STATION
PHOSPHATE ELIMINATION
FACILITY
HUb ISLAND
1km
Fig. 2. Location and bathymetry of Lake Tegel, Berlin.
resource for ground water replenishment and bank infiltration, supplying a fifth
of Berlin's drinking water needs, and plays an important role for fishing, shipping
and recreation (Heinzmann and Chorus, 1994).
Until 1985, Lake Tegel was supplied by two heavily polluted inflows which
produced hypertrophic conditions in the lake and yearly formations of blue-green
algal blooms. The phosphate input into the lake was reduced by more than an
order of magnitude by treating the inflows in a phosphate elimination facility,
which began operation in 1985. Maxima of phytoplankton biomass were transiently phosphorus (P) limited in 1989 at total P concentrations of <60 ug I"1, but
a pronounced and lasting impact of restoration upon phytoplankton began only
in 1994 with total P concentrations of <30 ug h 1 from May to August.
Hypolimnetic aerators were used in the lake from 1980 through 1991 to combat
anaerobic conditions in the hypolimnion, but these were used only occasionally
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K.-E.Lindenschmidt and LChorus
over the study period [for more detailed information on aeration, its modeling
and its effect on phytoplankton populations, refer to Lindenschmidt and Hamblin
(1997), Lindenschmidt and Chorus (1997) and Lindenschmidt (1998)], hence,
these years can be used to study the effects of chiefly natural fluctuations of water
column stability on the phytoplankton community.
Field and laboratory methods
Field sampling occurred in weekly to fortnightly intervals during summer and
monthly intervals in winter at the deepest site in the lake. Temperature profiles
were measured with electrodes (WTW, SYLAND). Phytoplankton samples were
taken from 2 m depth with a slow pump and immediately preserved with Lugol's
iodine solution. Nutrient samples were filtered with a 0.45-um-diameter membrane in the laboratory within 2-4 h of sampling.
Taxa were determined to the species level wherever possible. Centric diatoms
were enumerated by size classes rather than by species because recognition
cannot be certain for every cell counted. Aulacoseira spp., however, comprised
largely of A.granulata. Cryptophyceae were not further differentiated because
clear morphological criteria were dubious in most samples. Microcystis spp.
cannot be distinguished as individual cells in samples sonicated for counting, but
in Lake Tegel, these chiefly encompass M.aeruginosa, with very minor shares of
M.wesenbergii and M.flos-aquae, which justifies treating them as one species for
diversity and similarity calculations.
Phytoplankton were counted using an inverted microscope according to the
method of Utermohl (1958) at a magnification of X400 [see Chorus and Schlag
(1993) for details]. Biovolumes were derived from cell numbers and mean cell
volumes on the basis of measuring 10-20 cells (depending on the variability of
dimensions) of the species counted and calculating their mean cell volume using
geometrical models. For filamentous species (Planktothrix agardhii, Aphanizomenon flos-aquae and Aulacoseira spp.), total filament length within the diagonals was determined instead of counting cell numbers. Microcystis colonies were
disintegrated prior to counting in order to enable enumeration of single cells.
Samples for total phosphate were digested and determined spectrophotometrically by the formation of a molybdate-phosphate complex after reduction
by ascorbic acid. Ammonium and nitrate were measured using Dr Lange cuvette
tests: for ammonium, type LCK 304 (range 0.015-2 mg I"1 NH,-N) or LCK 305
(range 1.0-12 mg I"1 NH4-N) was used; for nitrate, type LCK 339 (range 0.23-13.5
mg I"1 NO3-N) or LCK 340 (range 5-35 mg I"1 NO3-N). Samples of total dissolved
silicate were digested using sulfuric acid and ammonium molybdate, and determined after successive reduction by tartaric acid and ascorbic acid.
Parameterization of water-column hydrodynamics
The lake number (Imberger and Patterson, 1990) is a non-dimensional ratio of
the buoyancy forces in the lake due to stratification to the external forces applied
to the water column, such as wind, that act counter to the buoyancy forces.
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Effect of water column mixing on phytoplankton
Lindenschmidt and Chorus (1997) described these forces as moments around the
center of volume of the lake: the mass moment MM applied by the density difference in the stratified water column and the wind moment WM applied by the wind
blowing along the lake surface. The lake number LN becomes:
LN = MM
WM
(1)
Forces due to Lake Tegel's inflows and outflows were not incorporated in this
study because their flow velocities are very small and their influences are localized. Forces due to aeration were also excluded from the parameterization since
aeration was in operation only for 1 day each in 1993 and 1994, and its contribution to the overall yearly mixing condition was deemed insignificant. Aerator
plume forcing was included in the study of non-continuous aerated years in
Lindenschmidt and Chorus (1997). The mass moment MM (Figure 3) may be
calculated as:
MM = M g (z v - ZG)P
(2)
where M is the mass of the lake, g is the acceleration due to gravity, Zv is the
height of the center of volume from the lake bottom, zG is the height of the center
of gravity and 0 is the angle the chord ZG~ZV makes with the vertical. 3 may also
be taken as the angle between the metalimnion and the water surface at the point
of upwelling:
(3)
where z T is the maximum height (or depth) of the lake, zM is the height of the
metalimnion and ^lA(zr) is a scaled fetch length with A(z-r) being the area of the
wind
—
2 « ,-, \
^
POU:A(ZT)
Fig. 3. Balance of forcing moments, wind and water mass, acting upon an idealized water body.
1933
K--E.lindenschmidt and I.Choras
lake surface. The term M g(zv - ZG) is equivalent to the potential energy PE
stored in the density profile:
PE =
ffp(z)gA(z)(z-Zv)dz
(4)
where p(z) is the density of the water and A(z) is the surface area; both are a
function of z (vertical coordinate from the lake bottom). A measure of the
strength of stratification is the amount of potential energy stored in the density
gradient relative to the center of volume.
The wind moment WM due to the wind forcing acting about the lake's center
of volume is calculated from (Imberger and Patterson, 1990):
WM = Pou.2A(zT)(zr-zv)
(5)
where p o is the density of the hypolimnion and M. is the surface water friction
velocity due to wind stress. It is assumed that the force applied by the wind
Po u*2 A(ZT) is constant over the entire lake surface.
Lake numbers equaling one indicate a balance between wind and buoyancy
forces. For very large lake numbers, the stratification is severe and dominates the
forces applied by the wind. For small lake numbers, the reverse is true. Intermediate values mean that either the wind forcing is very strong, the stratification
is weak, or both. Strong mixing in the epilimnion will also occur for lake numbers
somewhat greater than one. Hence, the lake number gives a good indication of
the relative turbulence and stability conditions in the water column: low LN (<cl)
being turbulent and high LN (»1) being stable.
Since field temperature measurements were taken at most on a weekly basis,
the one-dimensional mixing model DYRESM (DYnamic REServoir Model)
(Imberger and Patterson, 1981) was used to calculate density profiles for lake
number computations on a daily basis. The model was calibrated and verified for
Lake Tegel by Lindenschmidt and Hamblin (1997), and gives a reasonably accurate description of the lake's thermal structure varying with depth and time. The
reader is referred to Imberger and Patterson (1981) for a detailed description of
DYRESM.
The years 1992,1993 and 1994 were investigated in this study. Density versus
depth profiles from the model were used to calculate the center of gravity and the
potential energy [equation (4)] of the stratification for each day. Metalimnion
depths were calculated from the maximum gradients of these density profiles.
These values are incorporated in equation (2) to compute the mass moments
exerted by the stratification on the water column. Mass moments were also calculated from density profiles converted from field temperature measurements for
comparison, which typically showed good agreement between the two (see
Lindenschmidt and Chorus, 1997).
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Effect of water column mixing on phytoplankton
Diversity and similarity of species composition
Diversity was calculated using the Shannon function to the logarithmic base 2:
where BVn is the biomass of a given species n, BVtot is the total biomass and N is
the total species count. Similarity was calculated using:
Similarityi = 2 • ^ ,+
where i signifies a sampling day and i - 1 the previous sampling day. When using
the similarity index, caution must be taken that the sampling dates are evenly
spaced in time. A higher similarity between samples will automatically be
obtained if sampling is carried out daily rather than weekly for the sample time
period. Since for practical reasons our sampling intervals were not evenly spaced
in time, the biovolumes were first interpolated to 2 week intervals before the similarity index was calculated. Two weeks were chosen as the most appropriate interval because this is approximately the time needed for populations to establish
themselves.
Zm:Zeu ratio
The Zm:Zeu (mixing depth:euphotic depth) ratio was calculated to incorporate the
light environment into the species succession analysis. The mixing depth was
taken to be the top of the metalimnion determined from the temperature profiles
of the lake. The euphotic depth was calculated from the Secchi depths multiplied
by a constant. Using field measurements of light-intensity profiles taken at weekly
or fortnightly intervals from May to November 1995 (Danowski, 1996) and correlating the Secchi depth readings with the calculated compensation depths, this
constant was determined to be 2.5.
Results
Nutrient limitation
Owing to treated sewage in the inflow, inorganic nitrogen concentrations were
always in the range of several milligrams per liter and never limited phytoplankton growth in Lake Tegel during the 3 years studied (Figure 4). However,
as sewage treatment introduced nitrification in late 1992, the relative share of
ammonium strongly declined in favor of nitrate during 1993 and 1994.
Gradual oxidization of the sediments due to nitrate was probably the key factor
which led to a reduction in phosphate release from the sediments and, in consequence, to a further decline in total phosphate from concentrations well above
1935
K.-E.Undenschinidt and LChoius
2000
100
1992
1993
1994
Fig. 4. Concentrations of major nutrients.
50 ug I-1 in 1992 to summer values in the range of 30 ug H and always below 35 ug
I"1 TP in 1994. This means a move from concentrations scarcely limiting phytoplankton biomass down to levels of substantial P limitation.
Silicate concentrations were never observed below 0.2 mg I"1 during the 3 years
studied, and usually ranged between 0.5 and 1.0 mg I"1. Half-saturation constants
for many diatom species are an order of magnitude lower (Kilham, 1977; Tilman,
1981). Thus, silicate limitation is unlikely to have limited diatom growth in Lake
Tegel.
Mixing and light conditions
The lake numbers, temperature isopleths, Zm:Zeu ratio, and the Secchi, euphotic
and mixed-layer depths were plotted in juxtaposition (Figure 5) to investigate the
mixing and light environments in the lake. Lake numbers calculated from model
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Effect of water column mixing on phytoplanlcton
density profiles and field temperature measurements are plotted together for the
sake of comparison, which typically shows a good agreement between the two.
The water column was always thoroughly mixed in winter and early spring in
all the years studied (LN <cl). There was some reverse stratification (LN > 1) in
January/February of all 3 years due to ice cover.
In 1992, stratification began in mid-April (LN > 1) and for 1 month thereafter
there were several intermittent strong mixing events in the lake. The temperature contours also demonstrate that the stratification was very weak during this
time. From mid-May until August, the water column was stable (LN » 1) and
the mixing depth gradually increased. In mid-August, the stratification was weakened and began to break down, as indicated by the decreased lake numbers. By
the beginning of September, the lake was nearly thoroughly mixed (LN < 1; see
also temperature isopleths). There was a brief phase of stability in September
(LN 5> 1) before continuous thorough mixing prevailed after the beginning of
October.
The same pattern was evident for the years 1993 and 1994, although some
differences occur in the lake number profiles for the summer stratified period. In
1993, there was more intermittent strong mixing within the epilimnion (LN —* 1).
The temperature isopleths show that many secondary thermoclines developed
during the more stable periods, which broke down during the strong intermittent
mixing events. For 1994, intermittent epilimnion mixing occurred in the first half
of the stratified period until the end of June; the second half was very stable until
mid-August. A very hot summer resulted in higher water temperatures compared
to the previous 2 years. The smoother contours are indicative of less forcing due
to wind.
In winter and early spring of all 3 years, the Zm:Zeu ratio typically increased
(linearly) due chiefly to the reduction in the euphotic depth with the increase in
phytoplankton growth. As would be expected, this ratio declines drastically upon
the commencement of summer stratification when the mixing depth decreases
very rapidly. This may qualify as a very strong disturbance in the aquatic environment. The Secchi depth progressively increased to its highest spring/summer
value -2-3 weeks after stratification began. The year 1992 is an exceptional case
when the initial stratification was weakened and broken down due to strong
mixing before stable conditions persisted after the end of May. Interestingly, this
year shows two maximal peaks in the Secchi depth readings, both -2-3 weeks
after the two initial onsets of strong stratification. This may indicate that the
spring clear-water phase may not be solely due to the increased grazing pressure
of zooplankton upon the phytoplankton, but that after the onset of stratification
(disturbance) there is also a transition when pre-stratification species settle out
of the epilimnion and are replaced by species more suited to stratified conditions
(and greater Zm:Zeu ratios).
After the spring plummet in all three studied years, Zm:Ztu shows an increasing trend throughout the summer. This is primarily due to the progressive
increase in the mixing depth, since the Secchi depths, and hence the calculated
euphotic depths, remained relatively constant. Owing to the very prolonged
stable conditions in 1994, the mixed depth became shallower than the seasonal
1937
K.-E.lindenschinidt and LChonis
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1938
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I
Effect of water column mixing on phytoplankton
thermocline (trend shown as a dashed line corresponding to a lower, steep gradient in the density profile) and, overall, the values for Zm:Zeu are lower than in the
summers of the previous 2 years. In Lake Tegel, the mixing depth (i.e. mixing
environment) appears to be a more sensitive variable than the euphotic depth
(i.e. light environment) for the Zm:Zeu ratio.
The oscillations in Zm:Zeu, particularly May/June 1992, August/September
1992, throughout the summer of 1993, and August/September 1994, are attributed
to intermittent mixing with Zm:Zeu peaks occurring at or immediately after a
strong mixing event. These oscillations are in unison (inversely) with the concurring oscillations of the euphotic depth, suggesting that a turbidity effect in the
epilimnion occurs with each strong mixing event.
At the end of August 1992 and 1993 and mid-August 1994 (due to aeration),
the stratification breaks down. Subsequently, Zm:Zeu declines rapidly because of
the increase in the Secchi depth. Thus, in late autumn, the euphotic depth
becomes the sensitive variable in the mixing/light condition in the lake.
Phytoplankton succession
Figure 6 gives an overview of total phytoplankton biovolume differentiated by
phyla. All three years show a characteristic pattern, with dominance of diatoms
in spring, followed by a clear-water phase in late May. Summer associations
always included some populations of diatoms, but their biovolumes were strongly
influenced by the mixing status of the lake (see below). Dominant summer taxa
were dinoflagellates and cyanobacteria in 1992 and 1993, and diatoms in 1994.
The lower biovolume maxima attained in 1994 were due to pronounced limitation
by total phosphate at concentrations below 35 jig I"1 total P throughout the
summer for the first year since restoration had begun in 1985. Lower biomass led
to increased transparency, especially in July and August, particularly as the
diatoms settled out of the very stable stratified epilimnion during July.
In order to investigate the effect of the mixing state of the lake on phytoplankton succession, the phytoplankton biovolumes of species which established
substantial populations in Lake Tegel were plotted in approximate order of their
seasonal appearance, together with lake numbers and the Zm:Zeu ratio, in Figure
7. A summary of the strategy type, r-K (sensu Sommer, 1981) or C-S-R
(competitor-survivor-ruderal) (sensu Reynolds, 1988), for each species, and the
corresponding mixing status of the water column favoring their growth, are
given in Table I.
For each year, vernal diatom succession typically began with the dominance of
large centric species (chiefly Actinocyclus normannii and Cyclotella spp.) and
smaller populations of small centrics (Stephanodiscus spp.) as well as Synedra
Fig. 5. Lake numbers, temperature isopleths, Secchi, euphotic and mixed layer depths, Zm:Zcu ratio,
and phytoplankton diversity and similarity for the studied years 1992-1994. Aeration key: (i) 2-7 July
1993: sporadic testing of aerators; (ii) 18 August 1993, 8:50-16:00: V2 aerators on 100% compressor
capacity; (iii) 25 July 1994: sporadic testing of aerators; (iv) 1-17 August 1994: all aerators on 60%
compressor capacity.
1939
K.-E.Lindenschmidt and I.Chorus
J
F
M
A
M
J
J
A
S
O
N
D
Cryptophyceae
| Dlnophyceae
Bacillariophyceae
Chlorophyceae
| Conjugatophyceae
Euglenophyceae
Cyanophyceae
I Crysophyceae
Xantophyceae
Fig. 6. Total phytoplankton bio volume in Lake Tegel by major taxonomic groups.
spp., while the Zm:Zeu ratio was still relatively low. In 1993 and 1994, these populations were accompanied by Nitzschia acicularis as the Zm:Zeu ratio increased to
three. Nitzschia acicularis was not present in the lake in 1992, perhaps due to the
rapid rate of Zm:Zeu increase before the onset of stratification. As mixing depths
suddenly decreased in April, most of these species vanished rapidly, the large
centric diatoms being the last species whose populations plummeted as stability
Fig 7. Water column stability as lake numbers, phytoplankton species biovolumes in approximate
order of seasonal succession and Zm:Zcu for the studied years 1992-1994. Anab = Anabaena spp., Aph
f = Aphanizomenon flos-aquae, Ast f = Asterionella formosa, Aul = Aulacoseira spp., Cen = centric
diatoms with diameters <8,8—15 and >15 um, Cer = Ceratium spp., Chlo = Chlorophyta, Cry = Cryptophyceae, Diat = Diatoma elongatum. Frag = Fragillaria crotonensis, Lim = Limnolhrix redekei, Mic =
Microcystis spp., Moug = Mougeotia spp., Nitz = Nitzschia spp., PI ag = Planktothrix agardhii, Syn =
Synedra acus and Synedra spp., Trib = Tribonema sp.
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K.-E.Undenscbiiiidt and LChorus
Table L Strategy type, r-K (sensu Sommer, 1982) and C-S-R (competitors-survivors-ruderals; sensu
Reynolds 1988), and preferred mixing state of the water column for each species in Lake Tegel (see
also Lindenschmidt and Chorus, 1997)
Species/group
r-K
C-S-R
Source
Miring/stability condition in
Lake Tegel
Actinocyclus normanii
towards K
R
Sonuner (1981)
authors
authors
Sommer (1981)
Reynolds (1997)
Sommer (1981)
Reynolds (1997)
Sommer (1981)
Reynolds (1988)
Reynolds (1997)
Reynolds (1997)
Reynolds (1997)
Sommer (1981)
Reynolds (1997)
authors
Reynolds (1997)
authors
continuous mixing
(centrics <}> > 8 um)
Anabaena spp.
S
towards K
C-S
Aphanizomenon spp.
towards K
Aphanizomenon
flos-aquae
Asterionella formosa
Aulacoseira spp.
Ceratium spp.
Chlorophyceae:
Ankyra spp.
Coelastrum spp.
Monoraphidium spp.
Oocystis spp.
Cryptophyceae:
Chroomonas spp.
towards K
C-S
r
r
K
r
S
R
R
S
C
C
C
C
r
C
Cryptomonas spp.
Cyclotella spp.
C-S-R
towards K
(centrics <)> > 8 um)
Diatoma elongatum
C-R
towards K
R
Fragilaria crotonensis
towards K
Limnothrix spp.
Microcystis spp.
K
K
R
R
S
Nilzschia spp.
Planktothrix spp.
K
R
R
alsoS
Planktothrix agardhii K
R
alsoS
Slephanodiscus spp.
r
C
Sommer (1981)
authors
Reynolds (1997)
Sommer (1981)
Reynolds (1997)
Sommer (1981)
Reynolds (1988)
Sommer (1981)
Reynolds (1988)
Reynolds (1997)
Reynolds (1997)
authors
Reynolds (1997)
authors
Mure/al. (1993)
Reynolds (1988)
authors
Reynolds (1997)
prolonged stability
prolonged stability or mixing
intermittent mixing
prolonged mixing
prolonged stability
these species dominated,
with Cryptophyceae, after
the disturbance of initial
stratification
these species dominated,
with Chlorophyceae, after
the disturbance of initial
stratification
continuous mixing
intermittent mixing
intermittent mixing
continuous mixing
prolonged stability or
mixing
continuous mixing
intermittent and
continuous mixing
continuous mixing
(centrics <J> < 8 urn)
Synedra spp.
towards K
C-R
R
Synedra acus
Synedra ulna
towards K
towards K
R
Sommer (1981)
Reynolds (1997)
authors
Sommer (1981)
Sommer (1981)
Reynolds (1988)
continuous strong
mixing
in the water column increased (LN > 1). Smaller populations of Asterionella
formosa were also present in the spring and tended to show maxima in May when
stratification was stable.
In comparison of all 3 years, the spring diatom populations differed with respect
to the relative share of species. In 1992, when consistently low lake numbers
indicated pronounced mixing, only the large centric diatoms reached high
1942
Effect of water column mixing on phytoplankton
population densities. In 1993, when strongly oscillating lake numbers reflected
fluctuating mixing conditions with a fairly regular pattern of stable situations every
2 weeks, Synedra spp., Nitzschia acicularis and smaller centric diatoms also formed
substantial populations. 1994 shows a pattern between these two extremes with
dominance of the large centrics and lower shares of the other diatom species.
Generally, however, few of the diatom species were typical r-strategists (sensu
Sommer, 1981), most of them are more appropriately described as ruderals (sensu
Reynolds, 1988) with medium growth rates but high tolerance of low and varying
light conditions, as experienced through deep mixing in Lake Tegel.
Cryptophyceae were present with low biovolumes throughout, but showed
maxima in spring. In 1992, Chlorophyceae further diversified the phytoplankton
association, especially in May and early June, with minor biovolumes of two
species of Ankyra, two species of Coelastrum and Oocystis spp. Among the
cyanobacteria, Limnothrix redekei occurred during the spring overturn of 1993
with maximum biovolumes immediately before the onset of stratification.
Whereas the Chlorophyceae and Cryptophyceae may be classified as r-strategists,
L. redekei is another typical ruderal species.
Ceratium spp., the main dinoflagellates found in Lake Tegel, were present in
large amounts in July and August 1992 and 1993. The biovolume of this characteristic K-strategist with low loss rates (due to poor edibility by zooplankters)
peaks at the end of July and at the end of August 1992 during periods of water
column stability (LN > 1). The decreases in biovolumes between these peaks
coincide with more turbulent conditions (LN < 1). The large lake numbers during
mid-August 1993 indicate a higher degree of stability as compared to August
1992, which allowed more biovolume of this algae to form. In 1994, Ceratium spp.
developed only a small population, although the very stable conditions were
favorable for their growth.
The.bloom-forming cyanobacteria Microcystis spp. developed populations in
July and August 1992, and August 1993, during stable water column conditions.
Like Ceratium spp., it generally favors stable stratification. However, fluctuations
in population development suggest that this K-strategist was in strong competition with Ceratium spp.; many of its maxima and minima coincide inversely with
those of the Ceratium spp. populations. Microcystis spp. tended to tolerate more
mixing than Ceratium spp., as during the sharp increase in mixing in September
1992. Smaller populations of Microcystis spp. were able to persist into the autumn
when mixing became more frequent and prolonged, and Zm:Zeu was decreasing.
In 1994, Microcystis spp. developed a very small population during a prolonged
stable period in July and early August. After this, a substantial switch from very
stable conditions to strong mixing (enhanced by 17 days of aeration and reflected
by low lake numbers) caused its population to decline, although a stock was able
to persist into September [see Lindenschmidt (1998) for the effects of continuous,
intermittent and surge aeration on phytoplankton succession]. Aphanizomenon
flos-aquae and Aphanizomenon spp. coincided with Microcystis spp., but their
biovolumes were significantly lower (too low to quantify in 1994).
The midsummer diatom composition was dominated by Fragilaria spp. with a
very similar pattern in all 3 years. Its biovolume peaks sometimes occurred during
1943
K.-E.Lindenschmidt and I.Chorus
stable conditions, but always lagged behind strong mixing events in the epilimnion (especially in 1993 and 1994). Very likely, the larger population in 1993
was induced by the higher frequency of mixing events. Small numbers of Diatoma
elongatum were consistently present as well. Aulacoseira spp. (chiefly A.granulata), large diatoms which form filamentous colonies and have high sinking rates
due to their high specific density, were found in the lake in midsummer, especially
in 1993 and briefly in June of 1994. This is due to frequent events of strong epilimnetic mixing during both of these periods, which allowed these species to
remain in suspension. Generally, Aulacoseira spp. correlate (inversely) very well
with lake numbers during this time frame. In 1992, they did not appear in the lake
until autumn since prolonged quiescent conditions (LN > 2) prevailed in the
water column during the summer months. These clear connections of Fragilaria
spp. and Aulacoseira spp. to strong mixing events (lake numbers close to one)
demonstrate them to be characteristic ruderals. Surprisingly, Synedra spp. formed
a large population at the beginning of August 1994, whose maximum coincided
with increased turbulence in the water column induced by the surged aeration
event in August [see aeration event (iv) in Figure 5].
Anabaena spp. populations were present in Lake Tegel in July and September
1992 (coinciding with Microcystis spp. peaks) and July 1993 (shortly after Microcystis spp.). These consistently appeared in the lake when the water column was
stable, regardless of the duration of stable conditions [see also Lindenschmidt and
Chorus (1997) for results from 1989 and 1990].
Planktothrix agardhii, a typical K-strategist in lakes with shallow mixing (Mur
et al., 1993), appeared in the summer and autumn of these years with biovolume
peaks occurring during or immediately after strong mixing events, and population
declines (minima) occurring during periods of stronger stability. The summer
populations occurred after abrupt rates of increase in the Zm:Zeu ratios. The
autumn populations concurred with the maxima of the epilimnetic deepening
rate. Prior to 1992, when the lake was artificially aerated for the greater part of
the year (especially in summer), this species was not present. It appears that the
growth of P.agardhii is enhanced by intensive epilimnetic mixing, but does not
subsist when the mixing becomes too deep, as was the case in Lake Tegel during
artificial mixing by aeration (Lindenschmidt and Hamblin, 1997).
Autumn mixing led to the dominance of different species of large diatoms
(ruderals) during the 3 years studied. In 1992, the large centric diatoms (Actinocyclus normannii, Cyclotella spp. and Aulacoseira spp.) were the main phytoplankters during the same months. In 1993, Diatoma spp. appeared in large
numbers in the beginning of autumn, during strong mixing preceded by a long
period of prolonged and large stability. In the fall of 1994, Aulacoseira spp. were
the only diatom species to establish a significant population, with a maximum at
the beginning of September, after lake numbers had declined to nearly one.
Diversity and similarity
The diversity and similarity indices are plotted in Figure 5. Two forms of the similarity index calculations are given: (i) from actual sampling dates indicated by the
1944
Effect of water column mixing on phytoplankton
points and (ii) from interpolated values of the biovolumes on a fortnightly basis.
The latter is more representative of the actual similarity of species between the
now equispaced sampling dates and, hereafter, will be referred to as the similarity
index. These have been removed when the sampling dates correspond to actual
2 week intervals.
Figure 8 shows diversity plotted against similarity indices. The dominant strategist types (sensu Reynolds, 1988) are included for those days corresponding to
actual sampling dates. Points indicated with two strategist types represent a mix
of these species with the first type having a somewhat higher biovolume than the
second. In spite of the strong scatter, the points do form a concave-downward
bell-shaped function. C-strategists tend to be located between the middle and left
side of the bell (similarity < 0.75), and when they are the dominant type in the
algal population (no mix with other strategists) tend towards lower diversity (see
in particular 1993). S-strategists tend more to the right side of the bell (similarity
> 0.75), and when the algal population consists only of these types, also tend
4 *
3 "
C+R
2 ~
0
•
R_^-
°O
\
S R8 1
-«°o>R 1
/
o-
\°ss
i
1
I
i
i
'
1993
R
(
2 "
-
1
C. /
1
1
o-
°o>°^s%g
R#
Qo R*S-fe
oo
°o» S ^
/RtC»^\ o
\
R+C
1
^
A' °<^\
/C
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3 "
^
1992
1
1
1994
3 -
/
R.
2 "
/
/
'
R
/ °^
ooy V\
R+s
•
•*
/<S> ^-, ^ o/.
^
*O
1 •
1
0
0.0
0.5
•
1.0
Similarity
Fig. 8. Correlations between diversity and similarity for the phytoplankton populations in Lake Tegel.
Filled circles indicate sampling dates labeled with dominant strategist (sensu Reynolds, 1988).
1945
K.-E.Lmdenscfamidt and I.Choms
towards low diversity (particularly in 1992). R-strategists appear scattered
throughout the diagrams, but populations with R-C or R-S mixes tend to cluster
at the top of the bell with high diversity and an intermediate range of similarity.
This reinforces the C-R-S allocations in Figure 1 (top).
Understanding the impact of disturbances at an intermediate frequency upon
diversity and similarity seasonal patterns requires careful comparison with mixing
conditions, as indicated by lake numbers (Figure 5). In early spring, prior to the
onset of stratification, the diversity and similarity indices were high, due to the
co-existence of several species of diatoms (especially in 1993 and 1994) together
with cryptophytes and in some of the years also chlorophytes and/or L.redekei.
Successional trade-offs between these species require longer time spans during
this cool season, which results in fairly high values for similarity on a fortnightly
basis.
Initial lake stratification, a pronounced disturbance of the previously prevailing mixed conditions and indicated by the rapid increase in the lake numbers (LN
> 1) and steep decrease in the Zm:Zeu, caused a decline in the species diversity.
This decline was also accompanied by a decreasing trend in the similarity index,
which is most pronounced for 1993, and reflects the disappearance of a number
of the previously co-existing species as stratification began, leaving an impoverished association with some cryptophytes and/or chlorophytes. The situation
corresponds to that shown in Figure 1 for the phase immediately after a disturbance strong enough to eliminate the previously dominant species.
After the beginning of stratification in May and June of 1992 and 1993, stabilization of the water column progressed rapidly (LN » 1). The diversity shows an
increasing trend with similarity remaining low (Figure 5), indicating the gradual
establishment of new species in the lake after the onset of stratification. In the
same period in 1994, strong mixing events (LN < 1) in the epilimnion were numerous. The similarity index attains higher values than in the same time frame during
the two previous years, although diversity increased. This reflects the more
gradual transition from vernal to summer diatom populations with the large
centric diatoms still prevailing well into June (Figures 6 and 7).
From the beginning of June until mid-August 1992, the water column remained
stable for a prolonged period of time (LN » 1). This situation led to a decline in
diversity down to a midsummer low and a progressive increase in similarity
(Figure 5), due to the competitive exclusion of Microcystis spp., Anabaena spp.,
P.agardhii, Fragilaria spp. and, to some extent, the cryptophytes by Ceratium spp.
(Figures 6 and 7), and may be classified as a successional climax stage. Regular
and frequent mixing events after mid-August (LN = 1 ) caused diversity to
increase sharply and similarity to decrease. The dinoflagellates were replaced by
P.agardhii and Aulacoseira spp., both of which are more adapted to turbulent
conditions. The second large peak in the similarity index at the end of October,
accompanied by a decreasing diversity, indicates the competitive 'win' of these
species.
The summer of 1993 had many intermittent strong mixing events (LN
approaching one) and the diversity index remained generally higher than in 1992,
due to competition between Ceratium spp., Fragilaria spp., Microcystis spp. and
1946
Effect of water column mixing on phytoplankton
Plankthotrix agardhii, whose populations fluctuated throughout June and July.
The similarity index trend also remained high, reflecting the continuous presence
of these species. This means that intermittent disturbances prevented competitive exclusion between the phytoplankton species. Diversity reached a minimum
only once in early August when Ceratium attained a transient, but overwhelming,
biovolume maximum of almost 50 cm3 nr 3 without, however, excluding its
competitors or even significantly suppressing their biovolume. This may be
regarded as a typical example of vertical niche separation, because this population produced marked mid-day maxima at 2 m depth (data not shown). By late
August, diversity recovered as this population was declining, Microcystis spp. and
P.agardhii reached their maxima, and Diatoma spp. were growing.
In 1994, the diversity peak occurring at the beginning of July was preceded by
intermittent strong mixing in a relatively shallow mixing layer. These conditions
supported co-existence of Fragilaria spp., Diatoma spp. and Mougeotia spp.,
leading to rather high similarity between the associations from early June to early
July. The prolonged stable period from the beginning of July until mid-August
favored Mictocystis spp. but its population was kept at bay due to the surged aeration event in August [aeration event (iv) in Figure 5; see also Lindenschmidt
(1998)]. Similarity briefly declines, indicating some species changeover due to this
induced mixing and rapid mixed-layer deepening. A brief stable period at the end
of August and beginning of September caused a temporary rise in similarity due
to stable populations of Aulacoseira spp., P.agardhii and Cryptophyceae.
Discussion
In summary, 1992 was a year in which 3 months of stable conditions were long
enough to allow succession to proceed towards low diversity as a result of
competitive exclusion. In contrast, regular intermediate disturbances throughout
the summer of 1993 maintained an almost continuous high level of diversity. 1994
shows an intermediate position between these two extreme years with high diversity during the early summer phase of intermediate disturbance and a decrease
in diversity during late summer. However, 7 weeks of stable conditions apparently were too short for competition to reach a climax with low diversity.
Diatoms
Because of their higher density in comparison to other algal groups, diatoms
require well-mixed conditions in order to remain suspended in the water column.
Reynolds (1994) states that it is not the intensity of the turbulence, but the extent
of vertical mixing, which is so critical for diatoms. However, there are examples
where the intensity of mixing affects the outcome of species composition. Forsberg and Shapiro (1980) reported a dominance of cyanobacteria in a lake mixed
slowly due to aeration which was replaced by a diatom dominance when mixing
became more rapid.
Reynolds (1994) reports that Aulacoseira is the most rapidly sinking diatom,
but is able to tolerate some forms of mixing variability. Nixdorf (1994) indicates
1947
K.-E.Lindenschmidt and LChorus
growth of this algae in a strongly stratified water column. However, prolonged
stratification (3-4 weeks) caused the biomass to decline rapidly, even though
there was an ample supply of silica. This suggests that diatoms can grow in periods
of stability, if mixing occurs intermittently.
The results for the diatom populations for 1992 and 1993 show that increased
biovolumes are directly related to the duration and frequency of the periods of
intermittent strong mixing during stratification. Frequent mixing events are
required for these species to establish themselves and achieve large populations.
In nutrient-limited lakes, their growth will eventually lead to nutrient depletion
in the epilimnion. However, although diatom growth significantly depleted silicate concentrations in Lake Tegel, both silicate and total phosphate levels were
not low enough to limit them substantially. Mixing was not crucial to resupply
nutrients, but only to maintain diatoms in suspension. If a mixing event does not
occur for an extended length of time (>2-3 weeks), too many diatoms will have
escaped from the mixed surface layer and not enough stock will have remained
for the population to flourish once mixing does recommence. This model stresses
the importance of intermittence of stable and turbulent conditions for the
successful growth of diatoms. The data from Lake Tegel support this model by
showing that very prolonged periods of stability also affect the diatom population
negatively, as was the case in July/August 1994. In contrast, the two Fragilaria
peaks in July and August 1993, and the Diatoma peak in September 1993,
occurred immediately after week-long mixing times preceded by more stable
conditions. This reinforces the fact that it is not the stability or strong mixing
periods themselves, but the duration and frequency of the events, that allow
diatoms to attain large populations.
Dinoflagellates
Owing to their motility capabilities, dinoflagellates are able to migrate vertically
in the water column in search of nutrients and areas of optimum light intensity.
Stable conditions enable them to take full advantage of these capabilities. Dinoflagellates do need some turbulence, however, at the initial stages of population
growth in order for their cysts to be resuspended in the water column and an
inoculum to develop (Pollingher, 1988). The intermittent disturbances of strong
mixing before the expected dinoflagellate bloom in 1992 and 1993 were favorable
conditions for their establishment, and both years obtained relatively high biovolumes in July and August. Large populations were also established when periods
of turbulence in early July were followed by several weeks of stable conditions
(see Lindenschmidt and Chorus, 1997).
Cyanobacteria
Two cyanobacterial species, Microcystis and Anabaena, were particularly sensitive to changes in water column stability in Lake Tegel. They are the first bluegreen algae that established significant biomass in midsummers 1992 and 1993,
and their populations immediately plummeted during the abrupt transition from
1948
Effect of water column mixing on phytoplankton
stability to turbulence. However, Microcystis thrived in previous years under
conditions of strong mixing (Lindenschmidt and Chorus, 1997). This illustrates
that Microcystis can adjust to regular mixing better than to intermittent mixing.
Furthermore, a non-growing population can survive deep mixing well into the
autumn (Reynolds, 1984), especially if a significant stock already exists (Reynolds
and Walsby, 1975).
The literature is inconsistent as to the favored hydrodynamic conditions of a
water column for Limnothrix spp. and Planktothrix spp. Some studies show that
these species favor more turbulent conditions and appear in greater numbers
when Zm:Zeu is maximized (usually at spring and autumn overturn; Reynolds,
1994; Rojo and Cobelas, 1994). Examples from shallow lakes exist, however, for
Lredekei (Nixdorf, 1994) and P.agardhii (Rojo and Cobelas, 1994) where no
correlations with Zm:Zeu were observed. Nevertheless, it has been established
that Limnothrix and Planktothrix species are good light antennas and have the
highest adaptive capabilities to low average insolation of any algae (Reynolds,
1994). Also due to their sensitivity towards high light intensity, deeper mixing
reduces the risk of photoinhibition (van Liere and Mur, 1979). In Lake Tegel,
Limnothrix did appear in the spring when Zm:Zeu was at its maximum. The
dynamics of the Planktothrix populations, however, appeared to be more dependent on the rate change of the mixing and light environment in the water column.
Rapid increases in the Zm:Zeu ratios in summer were followed by population
peaks of these species. This was influenced more by the rapid decrease in the
euphotic depth rather than the mixing depth. The autumn population developed
large biovolumes when the rate of deepening of the mixed layer was at its
maximum. Although their growth rates are relatively slow, these species appear
to cope best with abrupt decreases in light availability.
Diversity and similarity
For Hamilton Harbor, Harris (1983) determined a correlation between the
changes in the phytoplankton community and changes in the physical structure
of the water column. Periods of constant overturn led to almost monospecific
blooms, whereas periods of intermittent mixing led to high phytoplankton diversity (Harris, 1986). This was also the case for Lake Tegel in all the years studied.
A substantial decrease in the diversity index occurred with the onset of summer
stratification, and the largest peaks were obtained in June and July after periods
of intermittent mixing. Thereafter,, prolonged stable conditions in the summer of
1992 and 1994 showed a decline in diversity. Frequent mixing events of the epilimnion in 1993 allowed the diversity trend to remain high. Prolonged water
column stability during summer stratification was accompanied by a large similarity index value by the end of the stable period. This concurred with a reduction in the diversity indicating the persistence and dominance of strong
competitors towards the end of a phase of competitive exclusion. With regular
frequent mixing in the epilimnion, both the diversity and similarity had relatively
high values, indicative of co-existence of 'ruderals' and K-strategists, and less
competition between, and exclusion of, species.
1949
K.-E.Undenscfainidt and LChorus
Conclusions
Using the model DYRESM, which was calibrated for Lake Tegel, allowed density
profiles to be calculated and a description of the stratification to be made on a
daily basis. Lake numbers could then be computed daily, which is necessary to
recognize disturbances an a time scale smaller than field sampling would allow.
The results fully confirm the predictions of the intermediate disturbance
hypothesis, showing that diversity was highest during phases of intermittence of
turbulence and stability at intervals of 2-4 weeks. Seasonal succession can
progress towards a climax stage of competitive exclusion and low diversity, as was
the case in Lake Tegel in 1992. However, in this fairly shallow and wind-exposed
lake, such situations are rare and the high frequency of ruderal dominance reflects
the impact of turbulence in the epilimnion.
Acknowledgements
The authors wish to thank the Meteorological Institute at the Free University of
Berlin for their kind provision of the meteorological data. Special thanks go to
Katrina Laskus for evaluating the phytoplankton, to Gertrud Schlag and Monika
Jung for creating Figure 7, and to Hans-Ullrich Wolf, Christa Kopplin and Elke
Pawlitzky for field sampling, chemical analysis and data management.
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Received on July 14,1997; accepted on May 14, 1998
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