competition between phyto- and bacterioplankton of lake balaton in continuous cultures

I Internat. Rev. Hydrobiol. I 83 1 1998 I 5-6 I 449-460 I

HESHAM M. SHAFIK'-*, ZOLTAN MASTALA' and LAJOS VOROS'

'Balaton Limnological Research Institute of the Hungarian Academy of Science, H-8237 Tihany, P.O.B. 35. Hungary

*Suez Canal University Faculty of Science, Department of Botany, Ismailia, Egypt

Competition between Phyto- and Bacterioplankton of Lake Balaton in Continuous Cultures

key words: phytoplankton, bacterioplankton, competition, carbon limited continous culture

Abstract

Aliquots of a water sample taken from the mesotrophic basin of Lake Balaton in August were incubated in three identical (2 liter) chemostats. Nutrients (35 pg POI-P . I-' week-' and 350 pg N03-N . I-' week-') were added by weekly pulses to the first culture and by continuous supply to the other two. The third culture was enriched continuously with Na-acetate (5 mg . I-' week-'). Pulsed nutrient supply resulted in permanent coexistence of three algal species (Mougeotia sp., Syedra acus v. radians and Lyngbya limnetica) while the continuous supply (second culture) led to the predominance of Lyngbya lirnnetica. The Na-acetate addition experiment showed, that in the absence of carbon limitation, picophytoplankton were able to compete successfully with bacteria. The results indicate that indigenous phytoplankton can only thrive when bacterial growth is limited by carbon.

I . Introduction

In most natural waters autotrophic and heterotrophic planktonic organisms compete for nutrient sources. Competition studies in chemostat cultures inoculated with natural phytoplankton assemblages, have clearly shown that under continuous nutrient supply, only as many species coexist as there are limiting factors (SOMMER, 1983; 1985). Other work has demonstrated that a pulsed nutrient regime can help to maintain the coexistence of more species and the frequency of nutrient addition affects the resulting species richness (ROBINSON and SANDGREN, 1983; SOMMER, 1985), competitive outcome and community structure (SAKS- HAUG and OLSEN, 1986) as well as cell size structure (TURPIN and HARRISON, 1980; SUTI-LE et al., 1987).

Planktonic bacteria are the most important heterotrophs in marine and freshwater pelagic ecosystems, possible utilizing the bulk of primary production (COLE et al., 1988; LAVAN- DIER, 1990). In Lake Balaton it has been estimated that about a half of the planktonic primary production is channeled through bacterioplankton on yearly basis (VOROS et al., 1996). Although planktonic bacteria play a key role in the degradation of organic carbon substra- tes, recent studies suggest that bacteria function as sinks rather than as sources of phosporus. GUDE et al. (1 992) failed to observe a net phosphorus transfer from bacteria to algae in natural water samples or to demonstrate this in culture experiments.

Many authors (e.g. CURRIE and KALFF, 1984; BERMAN, 1985; GUDE, 1991; THINGSTAD ef al., 1998) have suggested strong competition between algae and bacteria for phosphorus when the concentration of phosphorus is low. Fractionated uptake experiments with natural

Correspondence to: LAJOS VOROS

450 H. M. SHAFIK ef al.

plankton comunites showed that the concentration rather than the quality of the phosphorus source may be decisive for the outcome of competition for phosphorus between algae and bacteria (CODE et al., 1992).

The primarily P-limited phytoplankton of Lake Balaton (ISTVANOVICS et al., 1986) is extremely rich in algal species. Disregarding some extreme case, the diversity of phytoplankton has not been greatly reduced by eutrophycation (VOROS and NEMETH, 1980). The sediment of this shallow lake (mean depth of 3,5 m) is occasionally disturbed by storms from time to time. Phosphate desorption from the resuspended sediment may significantly contribute to the internal phosphorus loading (LIJKLEMA et al., 1986).

In the present study, the chemostat experiments with natural phytoplankton of Lake Bala- ton were conducted to examine the hypothesis that physical perturbations leading to peri- odic phosphorus release can contribute to the maintenance of high algal diversity. Experi- mental findings supported the hypothesis that allochthonous organic carbon load could influ- ence phytoplankton growth through phosphorus competition with planktonic bacteria.

2. Materials and Methods

2.1. Culture Technique

Three identical chemostats (A, B and C) of 2 liter capactiy were used. The chemostat apparatus is described in detail by SHAFIK (1991). A basic outline is given here. The culture medium was supplied from the reservoir to the culture vessel at the desired flow rate by a peristaltic pump (Masterflex 7523- 12) calibrated before use. The culture was aerated by pumping sterile air through a deeply inserted tube. The aeration also ensured the stimng of the culture. In addition, a teflon-coated magnetic stimng bar was used. All of the equipment and the culture medium had been autoclaved at 120 "C for 2 hours.

Filtered (GFF) natural lake water served as the inflowing medium. Nutrients (35 pg PO,-P. I-' week-' and 350 mg NO,-N. I-' week-') were added to the cultures. In the case of culture A this amount of nutrients was injected once per week. while in the cultures B and C the nutrient supply was continous. In addition culture C was enriched by 5 mg Na-acetate I-' week-' from a sterilized inflowing system.

A water sample taken from the mesotrophic basin of the shallow Lake Balaton in August was inoculated in all chemostats. The experiment was run at 24 "C corresponding to lake temperature at the time of sampling. The chemostats were continuously illuminated with 210 pE Einstein m-2 . s-' by cool- white light-tubes. A constant dilution rate of 0.2 d-' was used. This dilution rate is lower than the maximum growth rate of most planktonic algal species.

2.2. Chemical Measurements

Soluble reactive phosphorus (SRP), total phosphorus (TP), nitrate-nitrogen (N), total nitrogen (TN) were determined weekly, except in the case of culture A, where SRP and N were measured daily. SRP was measured according to MURPHY and RILEY (1962). T P was determined by the same method after digestion with mixed potassium persulphate-perchloric acid (modified from GALES et al., 1966). TN was oxidized to nitrate using the method of D'ELIA et al. (1977). Nitrate was determined via reduction to nitrite following ELLIOTT and PORTER (1971). Available silicon was measured at the beginning and the end of the experiment by the MULLIN and RILEY'S (1955) method.

2.3. Algal and Bacterial Measurements

From each culture 25 ml subsamples were preserved by LUGOL'S solution and stored in an ice-box (4 "C) until examination. Algal cells larger than 2 pm were counted by UNTERM~HL'S (1958) tecnique. The pico-sized algae (< 2 pm) were studied immediately from the fresh samples using an epifluores- cence microscope (Zeiss Axioplan) with blue excitation light (CARON. 1983).

Competition between Phyto- and Bacterioplankton 45 1

Bacterial cell numbers were determined by the acridine orange direct count method (HOBBI et al., 1977). Subsamples fixed with formaldehyde (final concentration 1.5%) were filtered through Sudan- black stained Nuclepore filters of 0.2 pm pore size. More than 400 bacteria were counted at 1250x magnification in a Zeiss-Axioplan microscope using blue (450-490 nm) excitation light.

Bacterial and algal cell volumes were estimated from length and width measurements and geometric formulas, a minimum number of 50 cells per samples were measured. Average algal cell volume (V) was computed by the following equation:

were: Vi is the volume and ni is the abundance of each species in the sample, N is the total phytoplankton abundance. The total biovolume of bacterio- and phytoplankton was converted to fresh weight (biomass) assuming a specific gravity of 1.0.

Phytoplankton carbon content (PCC) was calculated from total biovolume using the method of RKHA and DUNCAN (1985).

3. Results

The daily changes of SRP and N in the culture vessel of chemostat A (pulsed regime) show that the planktonic organisms took up the added P and N very rapidly (Fig. 1). SRP decreased to a low value in the 24 hours following addition, except in the third week. The concentration of the added N decreased by 64 f 5% in the 24 hours, except after the first addition, when the decrease was only 20%. Clearly the pulsed nutrient regime and the nutrient concentrations used cannot support a high biomass of bacterioplankton andor phytoplankton (see Figs. 3, 4 and 5) .

Both TN and TP were at a maximum on the first day and then decreased slightly in all chemostats to a level in agreement with the added nutrient concentrations, except for the last two measurements in chemostat A where no nutrients were added. Particulate phosphorous (PP) and particulate nitrogen (PN) were calculated from the differences between TP and SRP, and TN and N respectively (Fig. 2). PP and PN varied slightly in chemostat B. Che- mostat C was characterized by high PN until the second week of growth, when it decreased

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Figure 1. Daily levels of soluble reactive phosphorus (SRP) and nitrate-nitrogen (N) concentration in chemostat A .

452 H. M. SHAFIK et al.

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Figure 2. Changes of particulate phosphorus (a) and particulate nitrogen (b) concentrations in different chemostats.

significantly. The particulate N : P (by weight) ratios never fell below 8. All chemostats reached average particulate N : P ratio of about 10.5.

The soluble reactive silicon concentration of the added lake water was 3.4 mg . 1-'. At the end of the experiments, Si concentrations were 4.0, 3.34 and 3.29 mg . 1-' in chemostats A, B and C respectively. These measurements indicate that Si was not limiting nutrient in any chemostat.

The effect of different nutrient regimes became apparent from day 26. Fig. 3 clearly shows the effect of the addition of Na-acetate on the growth of bacterioplankton in chemostat C, where the biomass was about 400% higher than in the other chemostats. In chemostat A the average total bacterial biomass (TBB) was only about 51% and 12% of that measured in chemostats B and C respectively.

The bacterioplankton of chemostat C were characterized by the appearance of large coc- coid cells (1 p diameter) until day 21. Later the large cocci disappeared and long filamen- tous bacteria (0.7 p diameter) became dominant (Fig. 4).

Competition between Phyto- and Bacterioplankton 453

Figure 3. Effect of Na-acetate and inorganic nutrients (N and P) on bacterial biomass (chemostat A: pulsed N and P supply, chemostat B: continuous N and P supply, chemostat C: continuous N, P and

Na-acetate supply).

The average algal biomass was 74%, 86% and 17% of the total plankton (algae+bacteria) biomass in chemostats A, B and C respectively. The chances in total phytoplankton biomass (TPHB) and average cell volume are summarized in Fig. 5. In chemostat A the algae were the largest and the abundance was very low in comparison with the other chemostats. In this chemostat the cell volume of all dominant algal species remained unchanged, except for Syn- edra acus v. radians, whose cell volume doubled reaching 600 pm3. In chemostat B the average cell volume decreased until day 26, then remained unchanged, since Lyngbya limnetica dominated. Another pattern was observed in chemostat C, where the cell number increased, but average cell volume decreased dramatically as a result of the dominance of pico-sized algae with a cell diameter of 1 to 2 pm (Figs. 5 and 6’).

Diversity (SHANNON and WEAVER, 1949) was about 1.5 with the pulsed regime, but it was only 0.3 in chemostat B. Although the TPHB was the lowest in chemostat C the phytoplankton diversity was still high (H = 1.14).

In chemostat A green algae were represented by a Muugeotia sp. with high biomass (Fig. 6) and a large cell volume of about 1400 pm3. In addition different types of cyanobacteria (Cylindrospermpopsis raciborskii, Aphanizomenon jlosaquae, A. issatschenkoi and Lyngbya limnetica) and diatoms (Nitzschia acicularis, N. actinastroides, N. palea and Syn- edra acus v. radians) were found.

The highest TPHB with the lowest diversity was recorded in chemostat B. Biomass of green algae was very low throughout the period of investigation. Cyanobacteria increased and replaced the diatoms after day 21. The diatoms were represented by N. acicularis. Cya- nobacteria were dominant, mainly Lyngbya limnetica which reached more than 95% of the TPHB by the end of the experiment (Fig. 6).

The growth of phytoplankton in chemostat C was strongly affected by bacterioplankton. TPHB was very low, making up only 17% of the total planktonic biomass. The growth of green algae (only Mougeotia sp.) decreased. Pico-sized algae increased from day 14 to the end of the experiment. Maximum biomass of pico-sized algae was observed in the last peri-

454 H. M. SHAFIK er al.

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Figure 4. Effect of different nutrient regimes (see Fig. 3) on the succession of bacteria.


Figure 5 . Effect of different nutrient regimes (see Fig. 3 ) on algal biomass (a) and cell volume (b).

od of the experiment when it made up about 75% of TPHB. The biomass contribution of Lyngbya lirnnetica was not more than 1.3%. As regards variation in the growth of diatoms, only different species of Nitzschia were recorded (Fig. 6) .

4. Discussion

In chemostat A, where nutrients were added in pulses, the algae had exhausted most of the available P and N by the day after addition. The total phytoplankton biomass, the cell abundance and average cell volume decreased during the experiment, but the cell volume remained significantly higher than in the continuous nutrient regimes (chemostats B and 0. The pulsed regime enabled more species to coexist and thus maintained a higher diversity of phytoplankton than did the continuous nutrient supply. SHANNON'S diversity was the highest in the pulsed regime (H = 1.5) while in the phosphorus limited chemostat B tended to zero.

SHAFIK (1991) showed, that total biomass of algae was increased in an experiment on a water sample from Lake Balaton using the same nutrient concentrations with daily pulsed supply at 14 "C. In that experiment relatively higher diversity and domination of Nifzschia sp. (39% of the TPHB), Lyngbya limnetica (30%) and Synedra acus v. radians (29%) were recorded.

456 H. M. SHAFIK et al.

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Figure 6. Effect of different nutrient regimes (see Fig. 3) on algal community structure.


In the chemostat A the dominant species were Mougeotia sp. (60%). Synedra acus v. radians (21%) and Lyngbya fimnetica (16%). This result support the good competitive ability of planktonic Mougeotia. In multispecies chemostat experiments with Lake Constance phytoplankton it has been recorded as the best competitor for phosphorus after exclusion of diatoms by low Si : P ratios under steady state conditions (SOMMER, 1983) or higher Si : P ratios (SOMMER, 1985). In our experiment Si concentration was high in all chemostats and it has never been recorded as a limiting factor in Lake Balaton (SzAsz, 1989). We believe that nei- ther Si or Si : P ratio play an important role in the dominance of Mougeotia sp. This study and Sommer’s studies clearly show that Mougeotia sp. succeeds under a “low frequency” pulsed nutrient regime (weekly pulse). Its growth depends on a high P affinity, low half saturation constant of 2.3 pg P . 1-’ (SOMMER, 1986) and relatively large cell size 1400 pm’.

Members of Synedra genus proved to be the best competitors for P in many other experiments (SMITH and KALFF, 1983; KILHAM, 1986; SOMMER, 1987, 1988). This indicated that Synedra genus succeeds under “high frequency” pulsed nutrient regime.

In chemostat B both Mougeotia sp. and diatoms were completely excluded by Lyngbya limnetica, which dominated where nutrient addition was continuous but not organic carbon source was supplied. Bacterial cell volume was the lowest and its biomass decreased as a result of carbon deficiency.

Increasing the amounts of DOC (chemostat C) increased bacterial biomass. When bacterioplankton was growing well the growth of diatoms and also of other planktonic algae was dramatically decreased. This suggests that algae can only grow well when bacteria are growth limited by carbon or when their growth depends on algal excretion. Bacterial growth is regarded as carbon limited both in marine and freshwaters (GUDE etal., 1992; IETSWAART and FLY”, 1995). HEPINSTALL and FULLER ( 1994) suggested that bacterioplankton depend on algal carbon fixation by utilizing a significant portion of the released organic carbon as source of nutrients and energy for their growth and metabolic activity.

A conservative conversion factor between cell carbon content and volume (200 fg C + rn-’) was used to evaluate the significance of bacterioplankton in the inorganic phosphorus uptake assuming a C : P ratio of 80 reported by JURGENS and GUDE (1990). Using these conversion factors and total bacterioplanton biovolumes, the calculation resulted in 4.0, 2.2 and 28 pg bacterial P .1-’ in the last period of the experiment. These amount to 24%, 7% and 87% of the PP of the cultures A, B and C respectively. Clearly bacteria can only overcome algae in competition for phosphorus if they have access to a source of C that is not itself affected by P limitation. Those results are in agreement with ROTHHAUFT (1992). Bacterial biomass losses and concomitant nutrient release are reported from C-limitation but not from P-limitation (JURGENS and GODE, 1990).

The competition in chemostat C was mainly between bacterioplankton and pico-sized algae, which made up about 75% of TPHB. The dominance of phototrophic picoplankton (c 2 pm diameter) in chemostat C illustrates the well known inverse relationships between algal size and metabolic activity including the biomass specific phosphorus uptake (MALO- NE, 1980; SMITH and KALFF, 1983). As the bacteria have much higher affinity for phosphorus than algae (CURRIE and KALFF, 1984), if their growth is not carbon limited, they necessari- ly overgrow the algae. It seems only the picophytoplankton is able to compete with them more or less successfully. This hypothesis is supported by axenic culture experiments of a Synechococcus sp., isolated from Lake Balaton (MASTALA et uf., 1996). The half saturation constant (k) of growth of this cyanobacterium was 1.2 pg P . I-’ and maximum growth rate (pmax) was 2.3 d-’ (pmax/kE = 1.9).

No additional organic carbon source was added to chemostat A and B, therefore bacterial growth was probably limited by the reduced C available from algal exudation. This is pre- sumably more typical of natural water, as the case of greatest part of Lake Balaton, which lacks “extra” sources of available organic carbon. The western basin of the lake is different because it receives significant and increasing load of dissolved humic substances with the

45 8 H. M. SHAFlK ef a/.

parallel decrease of phosphorus load due to the wetland reconstruction on the watershed area. This increased and at least partly biologically available (V.-BALOGH and VOROS, 1997) organic carbon load probably supports the bacterioplankton growth and reduces phytoplankton growth by competition for limiting phosphorus resources.

5 . Summary

A summer water sample from the mesotrophic basin of a large shallow lake (Lake Bala- ton, Hungary) has been incubated in three identical chemostats at 24 “C with continuous illu- mination (210 WE . m-’ s-I). The dilution rate was 0.2 d-’. All chemostats were enriched with 35 pg POCP and 350 pg N03-N .1-‘. The first culture received weekly pulsed nutrient addi- tions while the others had continuous nutrient supply. In addition the third one was enriched by 5 mg Na-acetate I-’ week-’ as external organic carbon. Mougeotia sp. succeeds under a “low frequency” pulsed nutrient regime (weekly pulse). The growth of Mougeotia sp. may depend on a high P affinity, its low half saturation constant of 2.3 pg P and relatively large cell size. Synedra genus succeeds under “high frequency” nutrient pulses, while Lyngbya limnetica needs a continuous nutrient suppply to become predominant. In the absence of carbon limitation, mainly the pico-sized algae were able to compete for the nutrients with bacteria. The results indicate that the natural phytoplankton can only thrive when bacterial growth is limited by carbon. The growth of phytoplankton is P-limited, while bacteria may be carbon limited in Lake Balaton.

6. Acknowledgements

This study was partly supported by grant No. T 016348 of the Hungarian Research Fund (OTKA).

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Manuscript received January 20th, 1996; revised July 20th. 1998; accepted August 23rd, 1998

competition between phyto- and bacterioplankton of lake balaton in continuous cultures

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