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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 1927 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, 1928 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 1929 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 1930 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 1931 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. 1932 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). 1934 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 1936 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 •• •/• 71 s =• s - 1 (iu)iadsa 1938 (m) ifldoa naz-uiz 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. 1940 E661 5661 |aNos|v r r wvwj|r ON|OS v r r ^ v w j r a N O S v r r w v N d r c , 7" M 1 Vn r J_ ' ;::::.::Jf;::::::: 1 — ' ^j.n.i— : It 1 ~H IMdy T qui r, •WO T : *"* 1 1 r d!_ s | iiJUfa W 1 1 -so I :; t_ II..--. ti - --.. -s • , • - -~-r 1 1 -0 •-i'wW-w - o s 1 I Tl IT's ' -01 _ ^ ^ 0 -s fl-BMO £ nil t 1 •01 B >M*0 Mr 11Jir Mi in 111 nn 11HI \m T r u W ml LWF " < III HI III 1II ••IHMII IIIHHTI 1 ll'HH 1 * * -B 1 1 1 1 1IIMmII1 1 1 1 1 1 1 M l ONos]vrrt'wwd]roNosvr r i^vn J r a NO S vlrlr m V|AJ r f66l 2661 C661 no 2inznn aani 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 / 1 ~ 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. References ChorusJ. and Schiag.G. (1993) Importance of intermediate disturbances for the species composition and diversity of phytoplankton in two different Berlin lakes. Hydrobiologia, 249, 67-92. Cobelas,M.A. and Garcia-Moreto.C.R. (1990) Population dynamics of Nitzschia gracilis (Bacillariaceae) in a hypertrophic lake. Br. PhycoL / , 25,263-273. Connelly. 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