The dynamics of the phytoplankton community in the Barra Bonita Reservoir (São Paulo, Brazil) were studied through daily sampling in the field (integrated ...
Hydrobiologia 367: 139–152, 1998. © 1998 Kluwer Academic Publishers. Printed in Belgium.
139
Survival strategies of some species of the phytoplankton community in the Barra Bonita Reservoir (São Paulo, Brazil) A. C. A. Dos Santos & M. C. Calijuri Center for Water Resources and Applied Ecology, School of Engineering at São Carlos, University of São Paulo, C.P. 359, CP 13560-970, São Carlos, S.P., Brazil Received 21 May 1997; in revised form 15 February 1998; accepted 2 March 1998
Key words: phytoplankton, survival strategies, microcosms, tropical reservoir
Abstract The dynamics of the phytoplankton community in the Barra Bonita Reservoir (São Paulo, Brazil) were studied through daily sampling in the field (integrated samples from the euphotic zone) and microcosm experiments, for two short periods: the winter of 1993 (June 30 to July 10) and the summer of 1994 (January 24 to February 2). The goal of the study was to evaluate and compare the variations in the composition of isolated phytoplankton community which occur over short periods of time. Three series were separated into Erlenmeyer flasks for each study period, with samples from the euphotic zone divided into three portions: total, smaller than 64 µm, and smaller than 20 µm. All of the Erlenmeyer flasks were inclubated in situ at the sampling station. The maximum period of incubation was 10 d. Variations of the community in the euphotic zone were characterised by high diversity and a community in a state of non-equilibrium in winter, without the predominance of any species. In the summer, the community presented a low diversity and a state of equilibrium, with the predominance of Microcystis aeruginosa. The microcosm experiments showed that the confinement of the community in the Erlenmeyer flasks, and therefore in isolation from the physical variability of the ecosystem, especially in relation to the mixing patterns, stimulated the return of the community to the initial phases of succession with the predominance of small species and those which grow rapidly (r-selective or C-strategist).
Introduction The majority of the research which has considered the biomass and the variation in the composition of phytoplankton species has emphasised that the physiological and behavioural attributes of individual organisms or populations influence the variability of the community composition (Sandgren, 1988). Pianka’s (1970) concepts of r- and K-selection have been applied to the phytoplankton community by many authors, including Margalef (1978), Kilham & Kilham (1980), Sommer (1981), Harris (1986), Carney & Goldman (1988), and Arauzo & Cobelas (1994). These studies discuss the alternation of rand K-selection in the community assembles, proposing that the succession of species in the phytoplankton community is a predictable replacement of the
r species with the K species, from an unstable and mixed environment to a stratified and stable environment. Reynolds (1988a) updated the concepts of survival strategies for phytoplankton, relating them to ideas proposed by Grime (1979). According to Reynolds (op. cit.), phytoplankton can be divided into three groups of organisms with distinct but not necessarily mutual exclusive strategies: the C-strategists (pioneers), comprise species adapted to rapid reproduction and a superior ability to dominate the environment, as soon as the conditions become sustainable, partial exploiting environments saturated with light and nutrients; the R-strategist (runderaes), which are predominant in environments with great vertical mixing and are specialised to tolerate turbulent transportation and light gradients; and finally, the acquisitive
140 TAC, 1992) or to test theories such as the competition for resources (Sommer, 1985, 1988a, 1991). Although the answer found in this experiment cannot directly be used to explain what happens in the natural environment, the experiments in microcosms and the laboratory experiments can give important clues as to how the ecosystems work and the community relations (Fogg, 1875; Harris, 1986) and also the facility of manipulation. Therefore, the goal of this study is to better understand the survival strategies of the most abundant species isolated from environmental variability and the evolution of the community during short periods of time, in two times of the year in a tropical eutrophic reservoir. Description of the study site
Figure 1. Barra Bonita Reservoir (Calijuri et al., 1995).
S-strategists, species which tolerate stress or survive in environments with a severe restriction of essential nutrients. This division proposed by Reynolds (1988a) emerged because the studies which focused on changes in the composition of the species showed that the periods of mixing interrupt to expected progression from r- to K- strategists. Some more recent studies have already tried to use this new division (Sommer et al., 1993; Reynolds, 1996). As such, survival strategies are connected to the opportunities to respond to favourable environment and how each species adapts and relates to the others under the effects of environmental variability. The experiments in microcosm are an important tool to study the aquatic communities, because it allows us to control and even to eliminate the influence of some variables. Several experiments used microcosms with the aquatic community to study the succession and the productivity of organisms in laboratories (Odum & Hoskin, 1957; Ollason, 1997) to try to understand the effects of eutrofication through artificial fertilisation experiments (Løvstad, 1984; Henry et al., 1985), to toxicologic and physiological tests (SE-
The Barra Bonita Reservoir is the first of a series of six large reservoirs in the middle of the Tietê river, constructed with the objective of producing hydroelectricity. It is located at latitude 22◦ 290 S and longitude 48◦ 340 W, and is at an altitude of 430 m (Figure 1). This reservoir is located in the most populous and developed region of the interior of the State, bounded by the part of the Tietê Valley composed of the sections between the Pirapora and Barra Bonitas dams. The reservoir is formed primarily by the damming of the Tietê and piracicaba rivers, but also relies on input from innumerable minor and major tributaries. It is located in a transitional region between tropical and subtropical climates where the seasons are not well defined. The seasonal changes are not very pronounced, the clearest differences being between summer (the rainy season) and winter (the dry season, with little or no rain). During the hottest month (January) the maximum temperature is always above 22◦ C (the average temperature is 27◦C), and during the coldest month (July), the minimum temperature is below 19 ◦ C (the average temperature is 19◦C). The predominant rock in the region is basalt, and the drainage basin of Barra Bonita is predominantly constituted by purple latosoil. The vegetation in the region is dominated by monoculture sugar cane (Calijuri, 1988). The Barra Bonita Reservoir is a polymictic ecosystem with an average depth of 10.2 m, deeper than most of the reservoirs in the State of São Paulo. It is a eutrophic reservoir when the main external forces factors are rainfall, wind, flushing rate and retention time of the water. The retention time varies from 30 d to 6 months in different times of the year. The mixing
141 regime is mainly related to the effects of wind with alternating periods of turbulence and short-term stratification. During the rainy season, the input of nutrients occurs, as showed by Henry et al. (1985). According to them, phytoplankton is light limited during the rainy season due to large concentrations of suspended matter.
Materials and methods Intensive sampling (every day) was carried out during the periods of June 30 to July 10, 1993 and January 24 to February 2, 1994 at station 1, in the deepest part of the reservoir (Figure 1). Meteorological data (air temperature and precipitation) were made available by the CESP (Companhia Energética de São Paulo, the state electric company) at the Barra Bonita Reservoir. In order to evaluate the influence of environmental variability on the structure of the phytoplankton community, microcosm experiments were conducted during the two sampling periods. The microcosms were set up according to the following steps: • The depth of the euphotic zone was determined on the first day of sampling by radiation profiles obtained with a ‘quanta-meter’. Afterwards, the integrated sampling in the euphotic zone was conducted with the use of a vacuum pump, and 60 l of water were removed. • After homogenization, the sample was distributed into 30 2 l Erlenmeyer flasks, as follows: ten flasks contained the total community, 10 contained the community that passed through a net smaller than 64 µm, and 10 contained the community that passed through a net smaller than 20 µm. the separation in these fraction aims at separating the zooplankton from phytoplankton communities. • The Erlenmeyer flasks were closed, though permitting the entrace of air, and incubated on the surface of the water of the reservoir at the sampling station for at least 7 and at the most 10 d. Each day one flask from each series (with the total community, with smaller than 64 µm, and with smaller than 20 µm) was removed from the environment and taken to the laboratory. The physical and chemical parameters investigated were pH, alkalinity, (ASFA, 1985), and nutrients, total dissolved phosphates, nitrate, and reactive silicate, according to Mackereth et al. (1978), Strickland
Table 1. Average of the meteorological data in the periods of June 30 to July 10, 1993 (winter) and January 24 to February 2, 1994 (summer). Meteorological data
Winter
Summer
Air temperature (◦ C)
19.35 882.95 0.05 1.52 339.32 110.82
27.86 990.75 3.76 2.01 596.70 67.05
Solar Radiation (mE m−2 s−1 ) Precipitation (m m) Wind (m s−1 ) Outflow (m3 s−1 ) Retention time (days)
& Parsons (1960), and Golterman et al. (1978), respectively. Conductivity was measured in situ and corrected to 20. The profiles of the dissolved oxygen and temperature were done through the water check model T10 from Horiba Instruments. Phytoplankton samples for total counting were fixed with Lugol’s preservative. The identification of organisms was made under an inverted microscope (Zeiss), and the counting was made using the Utermöhl (1958) method. The statistical counting analysis was done according to the criteria proposed by Lund et al (1958), adopting 0.95 to confidence limits. Each cell was considered as a single one, except for Microcystis aeruginosa where the colony was considered as a single one. The identification of the species of the phytoplankton community was done using the classical and modern keys, general and to the specific groups, as mentioned by Dos Santos (1996). The calculation of the celular biovolume was done according to approximated geometric shapes as mentioned by Wetzel & Likens (1991), for each species was measured at least 20 and to most 50 ones. The concentration of chlorophyll a in each sample was determined spectrophotometrically (Nush & Palme, 1975). The diversity was calculated according to the Shannon-Weaver index described in Odum (1983).
Results The weather differences between the two sampling methods have already been discussed in Calijuri & Dos Santos (1996): these have been characterized as rainy summer and a winter without rain, as can be observed in Table 1.
142
Figure 2. Isolines charts of dissolved oxygen and temperature during winter (June 30 to July 10, 1993).
The variations of temperature and oxygen dissolved in water column presented a big difference in both periods with the presence of the summer stratification and the most homogenous column in winter, as can be observed in Figures 2 and 3. The variations in the concentrations of nitrate, total inorganic phosphate, and reactive silica are presented in Table 2. A total to 84 taxa were found. During the winter period, the most abundant groups in the euphotic zone of the reservoir were Chlorophyta, Cryptophyta, and cyanobacteria. Cryptomonas tetrapyrenoidosa was amongst the most abundant species during this period, followed by Monoraphidium tortile and Cyclotella stelligera, although none of these ever surpassed 50% relative abundance in any sample. At the end of the sampling period, the relative abundance of the cyanobacterian Microcystis aeruginosa increased, although without surpassing 30%. Other genera and species which also had abundance > 10% during some periods were: Gloeothece sp., Ankistrodesmus falca-
tus, Pseudanabaena catenata, Oocystis lacustris and Euglena sp. During the same period (winter), the microcosms isolated the unmodified community and the community smaller than 64 µm showed similar behavior, with the initial dominance of Cryptomonas tetrapyrenoidosa and Pseudanabaena catenata. The Chlorophyta totally dominated for two days of the experiment: this dominance occurred between the 5th and 8th days of incubation, and the main species were Pedinomonas minutissima and Monoraphidium tortile, the former with more than 80% relative abundance. On the other days of the experiment, before as well as after this period, the dominance was of Chlorophytes. However, this dominance was shared with Chrysophytes, once again represented by Chyclotella stelligera. In the microcosms that isolated organisms smaller than 20 µm, there was also a dominance of Chlorophytes, first Monoraphidium tortile and then Pedinomonas minutissima, which was followed by Cyclotella stelligera. The reduction in the initial population of Pseudanabaena catenata was reproduced,
143
Figure 3. Isolines charts of dissolved oxygen and temperature during summer (January 24 to February 02, 1994).
Figure 4. Relative abundance of the most abundant species in the integrated column of the euphotic zone and in the microcosms during winter.
144 Table 2. Average concentrations of nutrients in the integrated column of the Zeu, and in the microcosm experiments with the total community, that smaller than 64 µm, and that smaller than 20 µm, during the two periods of study in the Barra Bonita Reservoir. Days
Winter 1 2 3 4 5 6 7 8 9 10 Summer 1 2 3 4 5 6 7 8 9 10
NO3 (µg l−1 ) Zeu Tt M64
M20
PO4 (µg l−1 ) Zeu Tt
M64
M20
SiO2 (mg l−1 ) Zeu Tt M64
M20
1.20 1.26 1.01 0.98 1.12 0.99 0.99 0.79 0.99 0;97
1.10 1.22 1.11 1.15 1.10 0.76 0.89 1.15 – –
1.28 1.23 0.97 1.10 0.71 0.75 0.89 1.36 0.89 –
1.10 1.22 0.90 0.73 1.26 0.82 0.90 – – –
25.20 22.07 19.87 18.77 17.85 20.24 21.71 24.83 22.99 20.79
33.84 25.75 15.64 14.79 15.82 18.40 12.88 14.72 – –
29.06 18.95 14.54 13.62 16.19 16.56 13.62 13.43 11.78 –
28.32 19.68 14.54 13.80 12.33 16.74 12.15 – – –
3.55 4.23 4.03 3.79 4.92 4.63 4.43 3.79 4.33 3.18
4.07 4.39 3.35 4.22 4.50 4.58 4.18 3.80 – –
4.14 3.66 4.42 3.63 4.58 4.57 4.32 3.88 3.62 --
4.18 3.48 4.44 4.58 4.60 4.42 3.99 – – –
0.66 0.66 0.66 0.65 0.65 0.65 0.65 0.65 0.65 0.65
0.66 0.66 0.65 0.65 0.65 0.65 0.65 0.65 0.65 0.64
0.66 0.66 0.65 0.65 0.65 0.65 0.65 0.65 0.65 0.64
0.66 0.66 0.65 0.65 0.65 0.65 0.65 0.65 0.65 0.65
6.20 5.55 5.38 5.22 7.68 5.96 4.27 3.58 6.86 4.56
6.20 9.48 6.04 5.22 5.55 3.25 1.94 2.43 5.38 4.73
7.02 8.50 11.94 12.76 16.37 3.91 3.91 3.42 8.83 6.86
7.02 5.55 5.06 5.38 7.84 4.73 3.58 2.27 4.40 9.32
1.16 1.10 1.11 1.22 1.24 1.11 0.96 1.06 1.04 0.91
1.16 1.07 1.33 1.23 1.47 1.10 1.39 1.30 1.28 0.91
1.16 1.18 1.26 1.24 1.20 1.07 0.95 0.97 1.02 0.87
1.12 1.10 1.28 1.14 1.15 1.21 1.19 1.00 0.97 0.91
Figure 5. Relative abundance of the most abundant species in the integrated column of the euphotic zone and in the microcosms during summer.
145 although the same did not occur to the population of Cryptomonas tetrapyrenoidosa which sustained itself until almost the end of the experiment. Monoraphidium tortile and Cyclotella stelligera also showed increases in their populations, although no single species managed to dominate the community. The variation of the relative abundance of the most abundant species in the integrated column of the euphotic zone and in the experiments in winter can be observed in Figure 4. In summer, the dominance of the cyanobacteria in the euphotic zone was total. The species Microcystis aeruginosa dominated during the entire period, with a relative abundance of almost 90% on some days. In the microcosms which contained the total community, the dominance of the cyanobacteria Microcystis aeruginosa was also total, although it never surpassed a relative abundance of 80% in the community. In the microcosms Pedinomonas minutissima dominated again the community smaller than 64 µm in the summer, replacing the cyanobacteria Microcystis aeruginosa from the 5th day of incubation until the end of the period. Similar behavior was observed in the microcosms with the community smaller than 20 µm, with the replacement of Microcystis aeruginosa with Pedinomonas minutissima as from the 5th day and continuing until the end of the experiment. The relative abundance of the most abundant species in the integrated column of the euphotic zone and in the microcosm experiments during the summer can be seen in Figure 5. There were no significant differences between the concentrations of chlorophyll a in the winter and the summer in the samples from the euphotic zone. In the experiments in microcosms, only those which contained the community smaller than 20 µm presented a significant increase during the two periods. In the winter period, the increase of chlorophyll in the experiment with the community smaller than 20 µm took place on the 4th day, and in the summer after the 8th day. The variation in the concentration of chlorophyll in the euphotic zone and in the experiment during the two periods can be seen in Figure 6. The species diversity, calculated by the ShannonWeaver index, was on average greater in the winter than in the summer. In the winter, the diversity in the microcosms did not alter much when compared to the diversity in the euphotic zone. Only the experiment with the community smaller than 64 µm showed a significant drop as from the 6th day, rising again after the 9th day.
Figure 6. Concentrations of chlorophyll during the sampling periods (winter and summer).
Figure 7. Diversity (Shannon-Weaver Index) during the two sampling periods.
146 In the summer the diversity in the experiments was more differentiated than that observed in the euphotic zone. In the experiments with the total community, the variation in the diversity was small, only increasing significantly at the end of the period. In the microcosms with the community smaller than 64 µm and with the community smaller than 20 µm, the diversity had an initial increase until the 5th and 6th days, respectively, then falling to values much lower than those in the euphotic zone. The variation in the diversity in two samples periods can be observed in Figure 7.
Discussion Over the last decade, a large number of studies have been published showing that changes in the stability of the water column, in time intervals of about 10 d, are responsible for changes in the composition and maintenance of the diversity, and that the biomass and the taxonomic composition of the phytoplankton can change in a few days by changes in the mixing layer (Raynolds & Reynolds, 1985; Harris, 1986; Capblancq & Catalan, 1994). Comparing the two periods, the changes noticed in the environment seem to principally reflect the effect of meteorological factors, especially precipitation and temperature, influencing the physical structure of the ecosystem. The occurrence of precipitation in the summer would explain the greater concentrations of nitrate observed during this period, and circulation would be responsible for the greater concentrations of reactive silicate and phosphate during the winter. The bloom of Microcystis may also have contributed to the smaller concentrations of phosphate in the summer. During the winter, the community of the Barra Bonita Reservoir showed a constancy in the population of Cryptomonas tetrapyrenoidosa, although this species never had numerical superiority over the other species, its relative abundance always remained between 10–35%. Klaveness (1988) argued that the main controlling factor of the populations of Cryptomonas is the grazing by the microzooplankton, mainly rotifers, and that in the periods during or immediately after the occurrence of turbulence, the organisms of the Cryptomonadida group find favorable conditions to the establishment of their maximum population, since turbulence is responsible for the redistribution of nutrients in the water column and for the reduction of the pressure from grazing. Pautova et al. (1989)
and Istavánovics et al. (1994) found a large growth of Cryptomonas right after the end of the mixing period, slightly before the beginning of stratification. Other authors observed the development of Cryptomonas populations immediately after the occurrence of strong rains which destabilized the water column (Klaver & Mille, 1994; Romo & Miracle, 1995). Reynolds (1982, 1984b, 1996), in turn, states that Cryptomonas manages to survive in a large variety of environmental conditions, flourishing among the most common species in the mixing period as well as during in the stratification of the water column. Klavenes (1988) also argues that Cryptomonas spp. are found in temperate environments between the end of winter and the beginning of spring, during the detrital phase. They attain high rates of growth and respiration as a function of their small size and high area/volume ratio. Their survival strategy would be intermediate between those of the colonizing species (C- strategists) and the species which are tolerant of disturbance (Rstrategists), which would explain their survival over long periods in the water column. Other species which also have a relative abundance between 10–25%, such as Monoraphidium tortile, Ankistrodesmus falcatus, and flagellates such as Euglena, are smaller than Cryptomonas. According to Happey-Wood (1998), in all of the small green algae, such as the Chloroccocales and the small flagellates, the small size of the cell and a larger cellular area/volume ratio increase their capacity for nutrient absorption, which is an important adaptive advantage in oligotrophic waters, which have greater penetration of light and a low concentration of nutrients. Happey-Wood (1988) also proposes that Monoraphidium is an opportunist species, dominating in turbulent environments with a high availability of nutrients and light. Generally, Monoraphidium appearance coincides with that of the small diatoms, but reaches its peak immediately after the peak of the diatoms. Among the diatoms the most abundant species was Cyclotella stelligera, which took advantage of the greater concentrations of silica during the period, winter. According to Sommer (1988b), the diatoms occur during periods of circulation with high availability of nutrients and good light conditions and they grow quickly, mainly in the presence of high concentrations of nitrogen, being opportunists and colonizers (rstrategists and C-strategists). According to Reynolds (1984b), the growth of diatoms is mainly related to
147 two factors: the ratio of silica to phosphorous and the availability of light. For this author, Cyclotella is dominant in oligotrophic environments with great availability of light and a low Si:P ratio, if compared to other diatoms, such as those of the group of penales. Romo & Miracle (1994a), in a study in Spanish lakes, found the same genera found in this study. According to these authors, the presence of Cyclotella is associated with relatively low concentrations of silica and high concentrations of nitrogen and phosphorous; Monoraphidium would take advantage of periods of turbulence, and the distribution of Cryptomonas would be inversely related to the availability of light. In spite of the conditions being favourable to various species, the variability in the Barra Bonita Reservoir, mainly caused by the variation in the intensity of mixing, did not permit the predominance of any single species, occurring a constant alternation among the most abundant one, thereby increasing the diversity during the winter period. During the ten days of study in the winter period, the phytoplankton community presented greater diversity, most probably as a function of the variation in the intensity and frequency of mixing, leading to a community with a predominance of r-strategist species, or of C-strategists like Cyclotella, Monoraphidium, and Cryptomonas, species which are typical of the inital phase of succession. The confinement of the community to the microcosms, isolating it from the physical variability (mixing), led to variations in the species composition and dominance. This replacement of species seems to be related to the fact that Cryptomonas and Pseudanabaena, initially the most abundant species, are the most adapted to a low light regime, and when exposed to a climate of relatively constant radiation, their development is inhibited (Reynolds, 1984b). Furthermore, the confinement in Erlenmeyer flasks of organisms which were previously submitted and adapted to mixing conditions probably favoured the action of grazing mainly by rotifers. Various studies indicate that Cryptophyceas, and especially Cryptomonas, are an essential part of the diet of copepods and rotifers (Sterner, 1989). The maintenance of the population of Cryptomonas in the microcosms with the community smaller than 20 µm may be related to the absence of the pressure of grazing, since large predators were not a part of this community. Carrilo et al. (1995) argue that the presence of zooplankton in experiments of phytoplankton succes-
sion carried out in microcosms modifies the relative abundance of the species of the community, preying on those more subject to the action of grazing and reducing the competitive pressure for the other species. The effect of grazing reduces competitive pressure, provoked by the reduction of the population of Cryptomonas tetrapyrenoidosa, and which would lead to an advantage in species with faster growth such as Pedinomonas, Cyclotella, and Monoraphidium. However, even without the effect of grazing, as in the case of the microcosms with the community smaller than 20 µm, there was a modification of the community with the increase of the populations of Monoraphidium tortile and Cyclotella stelligera. For Monoraphidium and Pedinomonas, small size seems to have been the most important factor for growth under these conditions (Happey-Wood, 1988). Cyclotella may have benefited from a greater concentration of silica, because it is efficient in the absorption of other nutrients, especially phosphorous. All of these species are considered opportunists (r- or Cstrategists), presenting rapid growth and dominance of the environment when the conditions become ideal, as previously discussed. According to Sommer (1989b), in experiments with various species in integrated cultures, the flagellates are the first to disappear, while the cocoid algae dominate. Sterner (1989) reports that in some lakes the increase in the quantity of predators directly influenced the community, diminishing the dominance of algae such as Cryptomonas and stimulating the development of small green algae. In summer, the stability of the water column associated with an anoxic hypolimnion permitted the establishment of Microcystis aeruginosa as the dominant species in the Barra Bonita Reservoir (Calijuri & Dos Santos, 1996). The model for the dynamic of populations of Microcysts in temperate and subtropical environments, proposed by Reynolds et al. (1981), with the numerical superiority of this algae in the summer during the periods of high stratification, remaining in the sediment during the periods of mixing, has already been observed several times (Takamura et al., 1984; Bell & Ahlgren, 1987). Various hypotheses exist for the succession and numerical superiority of cyanobacteria in lakes, particularly Microcystis aeruginosa; these hypotheses range from the competition for nutrients (Holm & Armstrong, 1981; Vincent, 1989), better absorption of
148 carbon (Lucas & Berry, 1985; Shapiro, 1990), production of toxic substances (Lam & Silvester, 1979; Reynolds et al., 1981), reduction of the population losses (Kalff & Knoechel, 1978), decrease of the vulnerability to grazing (Porter, 1972; Haney, 1987), to the capacity to stay at the surface during periods of physical stability (Reynolds, 1984b; Humphries & Lyne, 1988). According to Calijuri & Dos Santos (1996), the presence of K-strategists (or S-strategists according to Reynolds, 1996), Microcystis was expected, considering the stability of the water column, as observed in Barra Bonita in the summer. Ganf (1974) attributed the presence of Microcystis in Lake George to the frequency of the daily alterations between microstratifications and holomixis. For Reynolds et al. (1987), the daily changes in the termal stratification and mixing in tropical lakes may favor the dominance of Microcystis. Reynolds (1984a) states that the appearance of ‘blooms" of Microcystis seems to be related to the occurrence of anoxia near the sediment. Calijuri & Dos Santos (1996) observed a significant population growth of Microcystis immediately after the period of anoxia in the bottom layers, occurring during the last days of the winter sampling. According to Calijuri & Dos Santos (op. cit.), during the summer the anoxia in the layers near the sediment was almost constant, resulting in a permanent liberation of phosphorus which must have favored the maintenance of the ‘bloom’ of the alga on the surface. In the summer samples, the dominance of the community by Microcystis aeruginosa was observed in the environment as well as in the microcosms which contained the total phytoplankton community, although there was a reduction of the population at the end of the experiment in these microcosms. This predominance seems to be related to the physical stability of the environment, unchanges in the microcosms. The colonies of Microcystis in the microcosms that contained the community smaller than 64 µm and 20 µm were smaller than the colonies found in the integrated column of the Zeu, and in the microcosms with the total community, which may be responsible for these organisms being more easily preyed upon by the microzooplankton, which would also have the advantage of being isolated from their larger predators. However, this hypothesis is limited by methodology, since in the microcosms with the community smaller than 20 µm there would not have been herbivorous zooplankton present. Only small protozoan could be part of this community (Margalef, 1976).
According to Reynolds (1984), Pedinomonas is an algae which takes advantage of the favorable conditions in the environment for rapid growth; it is known as an opportunist, having appeared in artificial fertilization experiments. The replacement of Microcystis with Pedinomonas may be associated with a better efficiency of nutrient absorption (Reynolds, 1996), though it is most probable that it is related to the lower competitive pressure resulting from the reduction in the populations of Microcystis in the microcosms with the community smaller than 64 µm and smaller than 20 µm. The concentration of nutrients was correlated with phytoplankton growth and no positive relation with nutients was found to explain the change in the species composition resulting from the competition for nutrients. It may be that more than one nutrient acted together, or that the action of some unanalyzed micronutrient was involved in this modification. Various studies point out the influence of more than one nutrient acting simultaneously. For the cyanobacteria, the influence of the N/P ratio is important in the determination of the growth of the population (Rhee & Gotham, 1980; Tilman et al., 1982; Sommer, 1985; Sommer et al., 1986; Turpim, 1988; Makulla & Sommer, 1993). This reduction in the populations of Microcystis, in microcosm containing a community less than 64 µm and 20 µm, may also be related to complex interactions with other organisms, such as protozoan and bacteria. Pearl (1988) stated that many cyanobacteria, Microcystis among them, interact with bacteria which may aid in the absorption of nutrients, or sometimes accelerate the process of degradation of the colonies; whether this interaction is beneficial or not for the cyanobacteria is not yet understood. Pearl (op. cit.) also stated that many protozoan form ‘blooms’ coinciding with the ‘bloom’ of cyanobacteria, but this relation is also not very well understood, being possible associated with either the predation of the cells of the phytoplankton or with the bacteria associated with these organisms. In Table 3, the most abundant species in this work were put, and their classification as to adopted strategy and the characteristics found in this work and in others on which to base the classification. In the summer, the stratified water column favored the K-selected species (or the S-strategist by Reynolds; definition, 1988b) in a community in equilibrium which showed characteristics of the final phases of succession. According to Sommer et al.
149 Table 3. More abundant species of the phytoplankton community, biovolume and survival strategies. Species
Average biovolume
Strategy
Characteristics
Microcystis aeruginosa
Cell: 150.53 µm3
K and S
Great size (colony). Stable water column or daily changes in the thermal stratification and mixing (Ganf, 1974; Reynolds, 1981; Reynolds et al., 1987; Calijuri & Dos Santos, 1996).
Colony: 48,982.44 µm3 Pedinomonas minutissima
19.88 µm3
r and C
Small size, fast growth, opportunist species. Common in artificial fertilization experiments (Reynolds, 1984a).
Cyclotella stelligera
68.95 µm3
r and C
Small size. Fast growth. Period of circulation and with availability or light (Sommer, 1988). Relatively low concentrations of silica and high concentrations of nitrogen and phosphorous (Reynolds, 1984a; Romo & Miracle, 1994a)
Monoraphydium tortile
12.11 µm3
r and C
Small size. Fast growth. Opportunist species, dominating in turbulent environments with a high availability of nutrients and light. (Harrey-Wood, 1988).
Cryptomonas pseudopirenoidifera
12,296.28 µm3
between
Middle size. Environments in the end of the mixing period, slightly before the beginning of stratification (Pautova et al., 1989; Istav´anovics et al., 1994). Development of populations immediately after the occurrence of strong rains which destabilized the water column (Klaver & Mille, 1994; Romo e Miracle, 1995). Low availability of light (Romo e Miracle, 1995). Common in the detrital phase (Klaverness, 1988).
R and C
(1993), a community in equilibrium is defined when (a) 1, 2, or 3 species of algae compose more than 80% of the total biomass; (b) this coexistence persists for more than 1 to 2 weeks, and (c) during this period the total biomass does not significantly increase. According to Reynolds (1996), the succession of sequential dominance of the phytoplankton is governed for a replacement of R-strategist species, which predominate in a state of mixing, with C-strategist species at the beginning of stratification, and then with S-strategists at the end of the period of stratification and the end of the succession. In this study, in the winter R-strategist species (Cryptomonas, Pseudoanabaena) were replaced in the microcosms by C-strategist species (Cyclotella, Monoraphidium, Pedinomonas). In the summer the replacement oc-
curred from S-strategist (Microcystis) to C-strategist (Pedinomonas) species. In general, it can be concluded that the confinement of the organisms in the microcosms was a disturbance which led the community to return to the beginning stages of succession (Reynolds, 1988b). This pattern was most visible in summer, since the natural community presented characteristics of the final phases of succession, with the predominance of large colonies with slow growth, K-selected and S-strategists, while in the microcosms these were replaced by phytoplankton organisms with small cells and a high growth rate, the opportunist r-selected and C-strategists, typical of the initial phase of succession. The Shannon-Weaver index showed that the winter period characterized by a non-stratified water column presented greater diversity than the stratified water
150 column in summer. According to Connell (1978) and Sommer et al. (1993), diversity increases with the appearance of disturbances and diminishes with stability. In the experiments in microcosms, the diversity of communities in both the winter and summer increased at first, but later presented a drop with the predominance of the rapidly growing species, such as Pedinomonas minutissima. This tendency may be better observed in the summer experiments, since the diversity of the initial inoculation was low due to the predominance in the environment of Microcystis aeruginosa. Reynolds (1996) argues that planktonic diversity is maintained by the frequent renewal to a more prime stage of succession, and that this community is subject to this process principally because of the physical variability of the system. In this study it was possible to observe that the increase in the stability, in both the environment and in the microcosms, led to a decrease in diversity. However, the return to the beginning of succession in the microcosms was always accompanied first by an increase in diversity. Acknowledgements The authors wish to express their thanks to Dr Milan Straskraba for the review and suggestions, to the National Research Council (CNPq), the São Paulo Research Foundation (FAPESP) and the São Paulo Electrical Company (CESP). References American Public Health Association, 1985. Standard methods for the examination of water and wastewater. Byrd Prepress Springfield, Washington, 1134 pp. Arauzo, M. & M. A. Cobelas, 1994. Phytoplankton strategied and time scales in a eutrophic reservoir. Hydrobiologia 291: 1–9. Bell, R. T. & I. Ahlgren, 1987. Thymidine incorporation and microbial respiration in the surface sediment of a hypertrophic lake. Limnol. Oceanogr. 32: 476–482. Calijuri, M. C., 1988. Respostas fisioecológicas da comunidade fitoplanctônica e fatores ecológicos em ecossistemas em diferentes estágios de eutrofização. Doctoral dissertation. PPG, Hidráulica e Saneamento, EESC, University of São Paulo, 293 pp. Calijuri, M. C. & A. C. A. Dos Santos, 1996. Short term changes in the Barra Bonita reservoir (São Paulo, Brazil): emphasis on the phytoplankton communities. Hydrobiologia 330: 163–175. Calijuri, M. L., M. C. Calijuri, L. Rios & J. G. Tundisi, 1995. The Use of Geographical Information Systems as a Tool for a Holistic View of Watershed and Reservoir Compartmentalization. Annual of the Ninth Annual Symposium on Geographic Information Systems. Vancouver, British Columbia, Canada: 697–703. Capblancq, J. & J. Catalan, 1994. Phytoplankton: which, and how much? In Margalef R. (ed.), Limnology Now: a paradigm
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