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Phytoplankton dynamics in a coastal saline lake (SE-Portugal)
Acta Oecologica 24 (2003) S87–S96 www.elsevier.com/locate/actoec
Phytoplankton dynamics in a coastal saline lake (SE-Portugal) Pedro Morais *, Maria Alexandra Chícharo, Ana Barbosa Faculdade de Ciências do Mar e do Ambiente, Campus de Gambelas, Universidade do Algarve, 8005-139 Faro, Portugal
Abstract The aim of this study was to characterise phytoplankton dynamics in a coastal saline lake, pinpointing putative biotic and abiotic regulatory variables of its succession and productivity. Between February and September 1998, samples for the analysis of physical, chemical and biological variables were taken fortnightly (except in February and April). The phytoplankton community showed three distinct periods of evolution. The first period (February-March) was characterised by a chroococoid non-colonial cyanobacteria bloom (maximum abundance, 4.3 × 109cells l–1) and also by its decaying. Long water residence and/or nitrogen limitation might have allowed cyanobacteria dominance; while its decaying could be associated to predation by aplastidic nanoflagellates and/or to the beginning of periodical partial renewal of lake water with water proceeding from an adjacent coastal lagoon (Ria Formosa). The second period (April-early August) can be differentiated, from the previous, by reduced abundances of phytoplankton (minimum abundance, 5.7 × 106 cells l–1) and plastidic nanoflagellates dominance. The overall low nutrient concentrations, likely as a consequence of periodical partial water renewal, could explain these results. In the last period (late August-September), increased phytoplankton abundance and the development of a diatom and mixotrophic dinoflagellate bloom was probably the result of a sudden increase in nutrient levels, occurring after a period of intense precipitation. In consequence, primary production reached a maximum value of 1367 mg C m–3 h–1; 36 times higher than a maximum value previously reported for Ria Formosa. © 2003 Éditions scientifiques et médicales Elsevier SAS. All rights reserved. Keywords: Phytoplankton; Succession; Productivity; Bottom-up; Top-down; Saline lake
1. Introduction Once phytoplankton was established as the major primary producer in aquatic environments (Raymont, 1980), one of the main goals of phytoplankton ecology has been the understanding of succession and productivity regulating mechanisms (Pennock and Sharp, 1994). Phytoplankton dynamics can be determined by bottom-up and/or top-down factors (Krebs, 1994). Bottom-up factors control species growth (e.g. light intensity, temperature, salinity, availability of nutrients, its ratios and chemical form), while top-down factors control its biomass (e.g. predation, viral lyses and parasitism) (Donk, 1991; Sherr and Sherr, 1991; Takahashi et al., 1982; Wehr and Descy, 1998). Phytoplanktonic blooms can be a consequence of seasonal processes (Goldman and Horne, 1983), natural (e.g. upwelling) (Moita, 1993) or cultural eutrophication (Hallegraeff, 1995). Cultural eutrophication is defined as the increase * Corresponding author. E-mail address: [email protected] (P. Morais).
© 2003 Éditions scientifiques et médicales Elsevier SAS. All rights reserved. DOI: 1 0 . 1 0 1 6 / S 1 1 4 6 - 6 0 9 X ( 0 3 ) 0 0 0 0 8 - 0
in nutrient concentration in any aquatic ecosystem, resulting in the degradation of its quality, as the outcome of antropic activities (Thompson and Rhee, 1992). The consequences have different intensities according to the available amount of nutrients, the ratios among them and the locality of its reception. The effects of these processes are problematic in confined places and/or with reduced water renewal (e.g. lakes, lagoons, rivers, inland seas) (Ketchum, 1983). In terms of this perspective, this study was undertaken in order to understand the causes that were behind the occurrence of some unpleasant situations, such as fish death and phytoplankton blooms, in the saline lake of Quinta do Lago (south of Portugal). This lake is located in a tourist resort, where some water activities take place. Speculations were made regarding the reason behind these situations, which spilled over the surrounding golf courses fertilisation. So, the objectives of this pioneer work in the saline lake of Quinta do Lago were to characterise, between February and September 1998, the phytoplankton succession and productivity, pinpointing the putative biotic and abiotic variables regulating its development and the evolution of the lake’s trophic state.
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2. Materials and methods 2.1. Study site This study took place in the saline lake of Quinta do Lago (SE-Portugal) (Fig. 1A), which has an area of 6.6 ha, a maximum depth of 2.9 m and an average depth of 2 m. It was carried out from February to September 1998. Fortnightly samples were taken, except in February and April, in three sampling stations (A, B and C) (Fig. 1C). This lake is situated in the west sector of the Ria Formosa Natural Park (Fig. 1B), and was a part of the Ria Formosa lagoon until 1972, when a ditch was built in order to create it. The lake is surrounded in the north by golf courses, in the east and west by houses and in the south by Ria Formosa; from where the water partial renewal for the lake’s water proceeds. Lake water management had two different approaches. Until the end of March 1998, partial water renewal was carried out in a 6-month period, during March and September high tides; afterwards, it was carried out every month, except in August 1998, during high tides. 2.2. Field work methods and laboratory analysis Sampling started between 09:30 and 10:30 h (GMT), except in the first sampling. Station A was the first to be sampled, followed by stations B and C, with a time gap of 45-60 min between each one. After sampling station C, 2 h and 30 min were required to execute the tasks described below. Every studied variable was investigated in each station, except protist abundance, analysed only in station C, the one that has the most complete record. In all the stations, the same sampling procedure was carried out. At every 50 cm depth, vertical profiles of temperature, salinity (probe Microprocessor Conductivity Meter LF196) and photosynthetic active radiation (PAR) (radiometer LI COR LI-1000 Data Logger; 4p sensor SPH Quantum) were made. At 1 m depth,
water samples were taken in a Niskin bottle for chemical and biological analyses. Immediatelyafter sampling, samples for dissolved oxygen concentration and primary production were prepared as meticulously described by Marques (1990). Primary production samples were incubated for 2 h and the method is based on the oxygen method first described by Gaarder and Gran. Oxygen concentrations were determined according to the Winkler method (Grasshoff et al., 1983). The net primary production determined in mg O2m–3 h–1 was converted to mg C m–3 h–1, considering that 1 mg of released oxygen corresponds to 0.313 mg of assimilated carbon (Strickland and Parsons, 1968). The remaining water sample was transferred to recipients with a silicone tube, once this material was established as not being toxic to organisms (Venrick, 1978a). Until sample processing, they were kept in the dark and cooled. On the land, samples for chlorophyll a were filtered through 0.7 µm pore filters (Whatman GF/F); the filtration pressure did not exceed 100 mmHg and the filters were kept frozen (–20 °C) until its spectrofluorimetric analysis (BMEPC, 1988). For the determination of five inorganic macronutrient concentration (ammonium, nitrate, nitrite, orthophosphate and silicate), 20 ml water samples were filtered through 0.45 µm pore cellulose acetate filters (MSI), preserved in 100 µl of saturated HgCl2 solution and were kept refrigerated (4 °C) until spectrophotometric analyses (Kirkwood, 1996), which were conducted according to the protocols of Grasshoff et al. (1983). Protist abundance was determined by applying two different methods. Microplankton abundance was determined with the Utermöhl method (Hasle, 1978), while nanoplankton abundance was determined using the Haas (1982) method. Samples analysed with the Utermöhl method were preserved with acid lugol (6.25% (v/v) final concentration), amplified 400× in a Zeiss IM35 inverted microscope and the cell counts were specified by Venrick (1978b). Samples analysed with the Haas method were preserved with glutaraldehyde 25%
Fig. 1. Geographical location of Quinta do Lago saline lake (A and B) and sampling stations’ spatial disposition (C).
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(2% (v/v) final concentration); stained with proflavin (Fluka), filtered, without exceeding 50 mmHg, through 0.45 µm black polycarbonate filters (MSI) and amplified 1250× in a Leitz DM LB microscope modified for epifluorescence. These two techniques were used because, with the Utermöhl method, autotrophic and heterotrophic taxa cannot be discriminated and others can be under- or over-estimated. With the Utermöhl method, the abundance of diatoms, dinoflagellates and cyanobacteria (except chroococoid forms) were determined, while chroococoid cyanobacteria, Criptophyceae, Prasynophyceae and/or Chlorophyceae abundances were inferred with the Haas method. The observed species were identified, if possible, to species level. The used nomenclature was based on the Tomas (1997) identification manual, but others were consulted (Dodge, 1982; Ricard, 1987; Sournia, 1986; Streble and Krauter, 1973). Autotrophic, mixotrophic and heterotrophic forms of dinoflagellates were established according to several authors (Gaines and Elbrächter, 1987; Lessard and Swift, 1986; Tomas, 1997). Mixotrophic dinoflagellate abundance was included in phytoplankton and phagotrophic protist analysis. 2.3. Meteorological variables Meteorological records concern the Patacão field station (Direcção Regional de Agricultura do Algarve), which is the nearest to the site of study. Atmospheric temperature data are expressed in a 10-d period average, while evaporation (class A evaporometer tub) and precipitation are presented in cumulative values of 10 d.
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Fig. 2. Nutrient limitation according to Si:N and N:P ratios. In each delimited section, nitrogen (N), phosphorus (P) and silica (Si) are ordered by decreased limitation degree.
3. Results The average atmospheric temperature varied between 12.4 °C (20 April) and 25.6 °C (10 August). The minimum atmospheric temperature was 5.5 °C (20 April) and the maximum atmospheric temperature was 34.0 °C (10 August) (Fig. 3A). Cumulative evaporation varied between 14.4 mm (10 February) and 102.3 mm (30 July). On 10 February, the highest cumulative precipitation was registered (80.5 mm); until 20 September, the total cumulative precipitation was scarce (50.5 mm), but in the last decade of September cumulative precipitation reached 65.2 mm (Fig. 3B), coinciding
2.4. Data processing and analysis The extinction coefficient was determined by converting the PAR profile data into logarithm and, according to the least squares method (Snedecor and Cochran, 1989), a linear trend line was adjusted to each profile; the extinction coefficient being the value of the slope. The average intensity of PAR in the mixed layer was determined (Kirk, 1986), taking into account the fact that the mixed layer depth is determined by the thermocline; however, in its absence, it corresponds to sampling station depth. The N:P and Si:N ratios were calculated and plotted on an XY logarithmic graph (Fig. 2), in order to determine the limiting element in the water (Rocha et al., 2002). Each limited area of the graph is expressed by the decreasing order of the limiting element. The trophic State Index related with chlorophyll a concentration (TSI (Chl a)), was used in order to examine the evolution of the lake’s trophic state (Carlson, 1977). TSI ranges between 0 and 100, varying from oligotrophic to hypereutrophic conditions (Carlson et al.). The main meteorological, physical, chemical and biological variables were inter-correlated with Spearman R non-parametric test. Bonferroni correction was applied to the chosen significance level (P < 0.05) to reduce the probability of significant casual correlations (Snedecor and Cochran, 1989).
Fig. 3. Maximum, average and minimum atmospheric temperature (A), evaporation and precipitation (B) registered in Patacão meteorological field station.
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Fig. 5. Temporal evolution of extinction coefficient (A) and average intensity of PAR in the mixed layer (B) in each of the three stations sampled. The arrows on top of graph A represent the moments of the lake’s water partial renewal. Fig. 4. Vertical profiles of temperature (A) and salinity (B) in each station.
with the beginning of a mixotrophic dinoflagellate and diatom bloom (Fig. 11). The water temperature oscillated between 17.6 °C (18 February) and 28.5 °C (21 August) (Fig. 4A). Salinity increased from 18 February (21.1) to 7 September (42.4) and had a decreased superior to 1 between 7 and 30 September (Fig. 4B). The entire vertical profile data show an absence of water column stratification (Fig. 4A, B). The extinction coefficient varied between 0.22 m–1(13 May) and 3.44 m–1 (30 September) (Fig. 5A), which coincided, respectively, with the minimum chlorophyll a concentration (Fig. 10) and the mixotrophic dinoflagellate and diatom bloom (Fig. 11). The average intensity of PAR in the mixed layer was between 87.8 µmol PAR s–1 m–2 (30 de September) and 1396.6 µmol PAR s–1 m–2 (22 April) (Fig. 5B). The dissolved oxygen concentration in the water varied from 1.66 ± 0.02 mg O2l–1 (7 September) to 9.77 ± 0.01 mg O2 l–1 (18 February). The similarity between stations was high, except in the last sampling (Fig. 6). Nutrient concentrations were, generally, less than 1 µM, apart from silicate concentrations which varied from 1.20 ± 0.09 to 17.68 ± 0.29 µM. At times, nitrate and orthophosphate
Fig. 6. Temporal evolution of dissolved oxygen concentration in each of the three stations sampled. The arrows on top of the graph represent the moments of the lake’s water partial renewal.
concentrations were slightly higher than 1 µM. Ammonium and nitrite concentrations were always less than 0.440 µM (Fig. 7A-E). If nutrients were limiting for phytoplankton growth, then Nitrogen (N) would have been the most limiting (Fig. 8). Phagotrophic protist abundance varied from 0.32 × 106cells l–1 (8 July) to 12.7 × 106 cells l–1 (30 September) (Fig. 9A). On 30 September, all phagotrophic protist groups presented its maximum abundances, except heterotrophic
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Prorocentrum minimum, a mixotrophic dinoflagellate, account for 62.5% (Fig. 9). Chlorophyll a concentration varied between 0.70 ± 0.00 µg Chl a l–1 (13 May) and 49.37 ± 2.00 µg Chl a l–1 (30 September). Generally, from 22 April to 21 August, the average concentration was less than 6 µg Chl a l–1. From 6 August to 30 September, chlorophyll a concentration increased 32.8 times (Fig. 10). The highest phytoplankton abundances were registered in late winter/early spring and in late summer/early autumn, while the lowest were found in between. Its abundance oscillated between 5.7 × 106cells l–1 (8 July) and 4.3 × 109 cells l–1 (18 February). From 18 February to 8 July, phytoplankton abundance decreased progressively, but between 11 and 25 March, a striking decrease was noticed, from 2.0 × 109 to 51.1 × 106 cells l–1. After 8 July, an increase in phytoplankton abundance was noticed until 30 September, when a relative maximum was registered (104.1 × 106 cells l–1) (Fig. 11A). From 18 February to 11 March, the phytoplanktonic community was dominated by chroococoid cyanobacteria, representing, respectively, 97.4 and 90.8%. After, and until the end of the study, autotrophic nanoflagellates were the most representative group, usually with relative frequencies greater than 98%. However, on 30 September, diatoms and mixotrophic dinoflagellates represented, respectively, 30.7 and 20.3% of the community, while autotrophic nanoflagellates represented 47.9% (Fig. 11B). The primary production variability between station was reduced, except on 30 September, when a maximum value of 1367.4 mg C m–3h–1 was registered (Fig. 12). TSI (Chl a) index varied from 7.1 ± 0.0 (13 May) to 68.9 ± 0.4 (30 September), which corresponds to oligotrophic and hypereutrophic levels (Fig. 13), following the evolution pattern presented by phytoplankton abundance (Fig. 11A). Spearman R correlation matrix (Table 1) shows significant correlations among some meteorological variables, namely water temperature, salinity, atmospheric temperature and evaporation. Dissolved oxygen in the water and mixotrophic dinoflagellates are significantly correlated, as aplastidic flagellates and autotrophic nanoflagellates. The highest correlations with primary production were obtained with temperature, nitrites and orthophosphates. 4. Discussion
Fig. 7. Temporal variations of ammonium (A), nitrite (B), nitrate (C), orthophosphate (D) and silicate (E) concentration in each of the three stations sampled. The arrows on top of graph A represent the moments of the lake’s water partial renewal.
dinoflagellates. Aplastidic flagellates were the most representative group of phagotrophic protists, with relative frequencies greater than 68.6%, except on 30 September when
In temperate lakes, the phytoplanktonic community is submitted to strong seasonal variations of biotic and abiotic variables. Thus, this community responds to those variations by presenting a different species composition, proportion and abundance. Usually, during spring, the community is dominated by diatoms; in summer, small flagellates and cyanobacteria have maximum abundances; through autumn and winter, the community is dominated by diatoms, dinoflagellates and cyanobacteria (Goldman and Horne, 1983); however, in Quinta do Lago temperate saline lake, this successional pattern was not verified.
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Fig. 8. Assessment of N, P or Si limitation in each sampling station. Note: Station A, data corresponding to 11 March and 6 August are not represented; Station B, data corresponding to 11 March, 13 May and 6 August are not represented; Station C, data corresponding to 22 April are not represented.
The reduced spatial variability of phytoplankton physiological variables and physical and chemical water variables, plus the absence of water column stratification, evokes the idea that there is only one water mass that allows the existence of only one phytoplanktonic population (Anderson et al., 1994). Phytoplankton dynamics presented three distinct periods, which can be inferred by the analyses of its abundance and composition, chlorophyll a concentration and the lake’s trophic state evolution. The first period (18 February-25 March) was characterised by long water residence, hypereutrophic and eutrophic trophic levels, the dominance of non-colonial chroococoid cyanobacteria bloom, and by its collapse and transition to autotrophic nanoflagellates dominance. In line with the bibliography (Hickel, 1985; Klemer and Barko, 1991; Meyer, 1994; Paerl, 1996), these cyanobacteria blooms usually occur in eutrophic and hypereutrophic aquatic systems, with periods of long water residence, months or even years. Long water residence in the lake, since September 1997, might explain the persistence of chroococoid cyanobacteria bloom, while its collapse could be related to the enhancement of the lake’s water partial renewal at the end of March 1998. Bloom collapse can also be related to top-down control (Goldman and Horne, 1983), maybe due to the maintenance of high and regular abundance of aplastidic flagellates, which are important consumers of cyanobacteria (Sherr and Sherr, 1991).
In the second period (22 April-6 August), the lake was subjected to mensal partial water renewal; the phytoplanktonic community was clearly dominated by autotrophic nanoflagellates and the lake’s trophic state oscillated between oligotrophic and mesotrophic. In lakes under oligotrophic conditions, phytoplanktonic species have reduced dimensions (Watson et al., 1997), so their high surface/volume ratio allows them to compete more efficiently for available nutrients than species of higher dimension, and therefore, to dominate the community (Anderson et al., 1994; Sommer, 1991). Predation losses are difficult to evaluate; once it could be reduced, due to low predatory population (Watson et al., 1997), or high when sustained by fast nanoplankton growth. Mensal partial water renewal might have influenced the maintenance of a certain species composition in the lake; once, during that period in Ria Formosa, the community was also dominated by autotrophic flagellates (Chícharo et al., 2000). However, phytoplankton abundance in the lake was always higher, probably due to more stable conditions in the lake, allied with optimal physical characteristics (Therriault, 1990), to higher predation rates in the lagoon, and perhaps because Ria Formosa nanoplankton was estimated only with the Utermöhl method, which might underestimate the lower fraction of plankton. During the last period (21 August-30 September), the increase in the lake’s trophic state to hypereutrophic condi-
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–1
Fig. 9. Evolution of total phagotrophic protist abundance (cells l ) (A) and relative frequency of each phagotrophic protist group (B). The arrows on top of graph A represent the moments of the lake’s water partial renewal.
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Fig. 11. Evolution of total phytoplankton abundance (cells l-1) (A) and relative frequency of each phytoplanktonic group (B). The arrows on top of graph A represent the moments of the lake’s water partial renewal.
tions, matched with the bloom of diatoms and mixotrophic dinoflagellates (P. minimum) and with high precipitation. It is important to state that during 1 month and 15 d, from late July to early September, the lake’s water partial renewal was not carried out. Until 7 September, the increase in waters residence, in addition to stable and optimal water temperatures, might lead to the increase in phytoplankton abundance and the lake’s trophic state. The subsequent water partial
renewal was not efficient once a phytoplanktonic bloom developed, probably as a result of intense precipitation. Severe eutrophication events are supposed to occur during late summer and early autumn (Strain and Yeats, 1999), usually as a consequence of high precipitation followed by periods of high insulation (Hickel, 1988). Primary production is also positively influenced by this conjecture (Paerl et al., 1999), perhaps as a result of introduced nutrients in the lake, which proceed from its drainage area. On 30 September, consider-
Fig. 10. Evolution of chlorophyll a concentration in each of the three stations sampled. The arrows on top of the graph represent the moments of the lake’s water partial renewal.
Fig. 12. Evolution of primary production in each of the three stations sampled. The arrows on top of the graphs represent the moments of the lake’s water partial renewal.
S94 Table 1 Spearman R correlation (P < 0.002) based on the most important variables obtained. The underlined correlations are significant for a significance level less than 0.002. ANF, autotrophic nanoflagellates; °C atm, atmospheric temperature; °C wat, water temperature; Chl a, chlorophyll a concentration; Cyano, cyanobacteria; Cili, ciliates; Crip, Criptophyceae; Diat, diatoms; DinA, autotrophic dinoflagellates; DinH, heterotrophic dinoflagellates; DinM, mixotrophic dinoflagellates; Evap, evaporation; FA, aplastidic flagellates; Im, average PAR intensity in the mixed layer; Ke, extinction coefficient; NH4+, ammonium; NO2–, nitrites; NO3–, nitrates; O2, dissolved oxygen; PO43–, orthophosphates; PP, primary production; Pra/Clo, Prasinophyceae and or Chlorophyceae; Prec, precipitation; Sal, salinity; SiO44–, silicates Sal
1 0.841 0.786 –0.269 0.407 –0.056 –0.566 0.538 –0.462 0.070 0.476 0.530 0.632 0.260 –0.390 –0.393 0.710 –0.531 –0.094 0.016 0.339 0.143 –0.275 0.066
°C atm
1 0.890 –0.354 0.104 0.245 –0.538 0.601 –0.429 0.252 0.564 0.568 0.484 0.154 –0.505 –0.531 0.564 –0.580 –0.050 –0.253 0.096 –0.160 –0.168 0.011
NH4+ NO3–
Evap
Prec
Ke
Im
O2
PP
1 –0.435 –0.049 0.503 –0.621 0.385 –0.610 0.154 0.597 0.441 0.258 –0.133 –0.742 –0.765 0.393 –0.605 –0.050 –0.302 0.303 –0.091 –0.374 –0.133
1 0.119 0.017 0.608 0.196 0.169 0.175 0.020 –0.217 –0.110 –0.273 0.232 0.511 –0.169 0.643 –0.080 0.558 0.327 0.154 0.116 0.249
1 –0.601 0.115 0.483 0.049 –0.273 –0.220 0.218 0.176 0.540 0.484 0.366 0.294 –0.019 0.055 0.731 0.008 0.124 0.132 0.448
1 –0.203 –0.018 –0.280 0.227 0.158 –0.035 –0.273 –0.625 –0.671 –0.750 –0.273 –0.203 0.309 –0.364 0.035 –0.551 –0280 –0.331
1 0.070 0.445 –0.140 –0.217 –0.204 –0.341 0.281 0.665 0.671 –0.349 0.825 –0.160 0.451 –0.039 0.091 0.523 0.470
1 0.042 1 0.073 –0.469 0.462 –0.242 0.457 0.069 0.287 –0.055 0.333 0.411 –0.049 0.610 –0.049 0.443 0.637 –0.019 0.070 0.635 0.067 0.011 0.2940.330 –0.238 –0.077 –0.488 0.056 –0.074 0.431 0.459 0.210 0.227
1 0.364 –0.436 0.378 –0.311 –0.343 –0.035 –0.350 –0.238 –0.130 –0.165 0.330 0.340 –0.536 –0.303
NO2–
PO43– SiO44– Chl a
ANF
FA
DinA
DinM DinH
Diat
Pra/Clo Crip
1 0.463 0.338 –0.021 –0.644 –0.306 0.355 0.050 –0.379 0.047 0.501 0.357 –0.237 –0.089
1 0.334 0.391 –0.163 –0.235 0.659 –0.030 0.044 –0.148 0.061 –0.336 0.192 0.336
1 0.801 –0.149 0.465 –0.061 0.498 –0.369 –0.003 0.492 0.541
1 –0.163 0.598 –0.414 –0.094 –0.039 0.377 0.253 0.387
1 –0.193 0.072 0.503 –0.048 0.044 0.281 –0.019
1 –0.300 –0.149 0.138 0.269 0.391 0.398
0.267 0.218 0.030 0.597
1 0.535 1 –0.570 –0.323 1 0.238 –0.078 0.288 1
1 0.323 –0.055 0.044 0.580 –0.297 –0.180 0.239 0.105 0.262 –0.226 –0.099
1 0.625 0.322 0.361 0.139 –0.262 0.505 –0.204 0.079 0.578 0.640
Ciano Cili
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°C Ág °C Ág 1 Sal 0.853 °C atm 0.900 Evap 0.938 Prec –0.463 Ke 0.074 Im 0.357 –0.655 O2 PP 0.462 NH4+ –0.649 NO3– 0.259 NO2– 0.470 PO43– 0.319 SiO44– 0.424 Chl a –0.046 ANF –0.641 FA –0.689 DinA 0.482 DinM –0.741 DinH 0.059 Diat –0.344 Pra/Clo 0.171 Crip –0.037 Ciano –0.315 Cili –0.235
1 1 –0.529 –0.654 0.398 –0.250
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Fig. 13. Evolution of Trophic State Index relative to chlorophyll a concentration in each of the three stations sampled. The arrows on top of the graph represent the moments of the lake’s water partial renewal.
able spatial differences were found in dissolved oxygen concentration and primary production; probably a consequence of high photosynthetic rate plus the time gap between sampling each station. Primary production has a positive correlation with nutrient availability (Raymont, 1980), however, in cases of nutrients saturation, temperature and light intensity are the key factors (Anderson et al., 1994), although light intensity could play a more important role (Raymont, 1980). The average intensity of PAR in the mixed layer did not explain primary production variation, so photoinhibition over phytoplankton growth might have occurred, once optimal values were not verified, since they were almost always greater than 300 µmol PAR s–1m–2 (Raymont, 1980). In Ria Formosa, the maximum reported primary production was 38.3 mg C m–3 h–1 (Falcão and Vale,1992), which is 36 times lower than the maximum found in the lake.
5. Conclusions In the saline lake of Quinta do Lago, physical, chemical and biological variables presented reduced variability and similar evolution, which suggests the existence of one water mass and one phytoplanktonic population in the lake. For these reasons, sampling in a central position could be considered in future studies. The increase in water temperature might have allowed phytoplankton to optimise its growth and productivity. However, high light intensity in the water column might have counteracted temperature increment effect over primary production by a process of photoinhibition. Nitrogen limitation might have been important in defining of phytoplankton communities, mainly during non-colonial chroococoid cyanobacteria dominance. A possible decrease in nutrient concentration, in relation with the period prior to the beginning of the study; predation of aplastidic flagellates on those cyanobacteria and water partial renewal were possi-
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bly in the origin of the bloom collapse. Afterwards, mensal water partial renewal and reduced nutrient concentration seemed to propitiate autotrophic flagellates the required conditions to dominate the phytoplanktonic community. At the end of the study, a possible entrance of nutrients into the lake, probably by runoff waters as a consequence of high precipitation, might have triggered the conditions for the development of the diatom and mixotrophic dinoflagellate bloom. Partial water renewal of lake water was probably important in defining a phytoplanktonic community similar to the one found in the western part of the Ria Formosa and in defining the lake’s trophic state evolution, mainly in its reduction and maintenance. However, partial water renewal was not efficient, in sustaining reduced trophic levels and in defining the structure of phytoplankton community, when intense precipitation matched with periods of high temperature and insolation.
Acknowledgements The authors would like to acknowledge Dr. Helena Marques, Mr. Fernando Braga and Mr. Artur for their helpful contribution during field work and especially to Ms. Ana Marques for her involvement during manuscript development.
References Anderson, A., Haecky, P., Hagström, Å., 1994. Effect of temperature and light on the growth of micro- nano- and pico-plankton: impact on algal succession. Mar. Biol 120, 511–520. BMEPC (Baltic Marine Environment Protection Commission), 1988. Guidelines for the Baltic monitoring programme for the third stage, Part D. Biological determinants, Baltic Sea Environment Proceedings number 27 D, Helsinki Commission, Helsinki, pp. 161. Carlson, R., 1977. A trophic state index for lakes. Limnol. Oceanogr. 22 (2), 361–369. Carlson, R., Chapra, J., Gerritson, G., Gibson, S., Heiskary, S., Jones, J., Nozik, M., Simpson, J., Smeltzer, E., 2003. Nutrient Criteria Technical Guidance Manual: Lakes and Reservoirs. US EPA Office of Water, Office of Science and Technology, USA. Chícharo, L., Chícharo, M.A., Gouveia, I., Condinho, S., Amaral, A., Miguel, C., Graça, C., Alves, F., Regala, J., 2000. Biological assessment of bivalve stocks of Ruditapes decussatus and Cardium edule in the Ria Formosa, Project DG XIV-97/106 final report, Faro, p. 88. Dodge, J.D., 1982. Marine dinoflagellates of the British Isles. Her Majesty’s Stationery Office, London, pp. 303. Donk, E.V., 1991. The role of fungal parasites in phytoplankton succession. In: Sommer, U. (Ed.), Plankton Ecology, Succession in Plankton Communities. Brock/Springer Series in Contemporary Bioscience, New York, pp. 171–194. Falcão, M., Vale, C., 1992. Variabilidade espaço-temporal e de maré na Ria Formosa: nutrientes e productividade primária da coluna de água. Resumos 1° Encontro sobre a Ria Formosa, Quinta de Marim, pp. 15. Gaines, G., Elbrächter, M., 1987. Heterotrophic nutrition. In: Taylor, F. (Ed.). The Biology of Dinoflagellates. Blackwell Scientific Publications, Oxford, pp. 224–268. Goldman, C.R., Horne, A.J., 1983. Limnology. International Student Edition, Tokyo, pp. 464.
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Grasshoff, K., Ehrhardt, M., Kremling, K., 1983. Methods of Seawater Analysis, second ed. Verlag Chemie, Kiel, pp. 419. Haas, L.W., 1982. Improved epifluorescence microscopy for observing planktonic microorganisms. Ann. de l’Inst. Océanog. 58 (S), 261–266. Hallegraeff, G.M., 1995. Harmful algal blooms: a global overview. In: Hallegraeff, G.M., Anderson, D.M., Cembella, A.D. (Eds.). Manual on Harmful Marine Microalgae. UNESCO, Paris, pp. 1–22. Hasle, G.R., 1978. The inverted-microscope method. In: Sournia, A. (Ed.). Phytoplankton Manual. UNESCO, Paris, pp. 88–96. Hickel, B., 1985. Cyanonephron styloides gen. et sp. nov., a new chroococcal blue-green alga (Cyanophyta) from a brackish lake. Algol. Stud 38 (39), 99–104. Hickel, B., 1988. Unexpected disappearance of cyanophyte blooms in Plubsee (North Germany). Algol. Stud. 50-53, 545–554. Ketchum, B., 1983. Enclosed seas-introduction. In: Ketchum, B.H. (Ed.), Ecosystems of the World, Estuaries and Enclosed Seas. Elsevier Scientific Publishing Company, Amsterdam, pp. 209–218. Kirk, J., 1986. Light and Photosynthesis in Aquatic Ecosystems. Cambridge University Press, Cambridge, pp. 401. Kirkwood, D., 1996. Nutrients: practical notes on their determination in sea water, ICES Techniques in Marine Environmental Sciences-no. 17, ICES, Copenhagen, p. 25. Klemer, A., Barko, J., 1991. Effects of mixing and silica enrichment on phytoplankton seasonal succession. Hydrobiology 210, 171–181. Krebs, C.J., 1994. Ecology: The Experimental Analysis of Distribution and Abundance, Fourth ed. HarperCollins College Publishers, New York, pp. 801. Lessard, E.J., Swift, E., 1986. Dinoflagellates from the North Atlantic classified as phototrophic or heterotrophic by epifluorescence microscopy. J. Plankt. Res. 8 (6), 1209–1215. Marques, M.H., 1990. Variação da produção primária do fitoplâncton na coluna de água e sua determinação, Relatório elaborado no âmbito das provas de aptidão pedagógica e científica. Universidade do Algarve, Faro, pp. 42. Meyer, B., 1994. A new species of Cyanodictyon (Cyanophyceae, Chroococcales) planktic in eutrophic lakes. Algol. Stud 75, 183–188. Moita, M.T., 1993. Spatial variability of phytoplankton communities in the upwelling region off Portugal. ICES, C.M., L (64), pp. 20. Paerl, H.W., 1996. A comparison of cyanobacterial bloom dynamics in freshwater, estuarine and marine environments. Phycologia 26 (6), 25–35. Paerl, H.W., Willey, J.D., Go, M., Peierls, B.L., Pinckney, J.L., Fogel, M.L., 1999. Rainfall stimulation of primary production in western Atlantic Ocean waters: roles of different nitrogen sources and co-limiting nutrients. Mar. Ecol. Prog. Ser 176, 205–214. Pennock, J., Sharp, J., 1994. Temporal alteration between light and nutrientlimitation of phytoplankton production in a coastal plain estuary. Mar. Ecol. Prog. Ser 111, 275–288.
Raymont, J.E.G., 1980. Plankton and productivity in the oceans. Phytoplankton, vol. 1. second ed. Pergamon Press, Oxford, pp. 489. Ricard, M., 1987. Atlas du phytoplankton marin. Diatomophycées, vol. 2. Editions du CNRS, Paris, pp. 297. Rocha, C., Galvão, H., Barbosa, A., 2002. Role of transient silicon limitation in the development of cyanobacteria blooms in the Guadiana estuary, South-Western Iberia. Mar. Ecol. Prog. Ser. 228, 35–45. Sherr, E.B., Sherr, B.F., 1991. Planktonic microbes: tiny cells at the base of the ocean’s food webs. Trends Ecol. Evol. 6 (2), 37–69. Snedecor, G., Cochran, W., 1989. Statistical Methods. Iowa State University Press, Iowa, pp. 524. Sommer, U., 1991. The role of competition for resources in phytoplankton succession. In: Sommer, U. (Ed.), Plankton Ecology. Succession in Plankton Communities. Brock/Springer Series in Contemporary Bioscience, , New York, pp. 57–106. Sournia, A., 1986. Atlas du phytoplankton marin, vol. 1: Introduction, Cyanophycées, Dictyochophycées, Dinophycées et Raphidophycées. Editions du CNRS, Paris, pp. 219. Strain, P., Yeats, P., 1999. The relationships between chemical measures and potential predictors of the eutrophication status of inlets. Mar. Pollut. Bull. 38 (12), 1163–1170. Streble, H., Krauter, D., 1973. Das leben im wassertropfen. Mikrokosmos Deustsche Mikrobiologische Geselscnatt, Stuttgart, pp. 336. Strickland, J., Parsons, T., 1968. A practical handbook of seawater analysis. Fish. Res. Bd. Can. Bull., Ottawa 167, 311. Takahashi, M., Koike, I., Iseki, K., Bienfang, P., Hattori, A., 1982. Phytoplankton species’ responses to nutrient changes in experimental enclosures and coastal waters. In: Grice, G.D., Reeve, M.R. (Eds.). Marine Mesocosms. Springer-Verlag, New York, pp. 333–340. Therriault, J.C., Legendre, L., Demers, S., 1990. Oceanography and ecology of phytoplankton in the St. Lawrence Estuary. Coast. Estuar. Stud 39, 269–295. Thompson, P.A., Rhee, G.Y., 1992. Phytoplankton responses to eutrophication. In: Rai, L.C., Gaur, J.P., Soeder, C.J. (Eds.). Algae and Water Pollution. E. Schweizerbart’sche Verlagsbuchhandlung, Stuttgard, pp. 125–166. Tomas (Ed.), C.R., 1997. Identifying Marine Phytoplankton. Academic Press, New York, pp. 858. Venrick, E.L., 1978a. Water-bottles. In: Sournia, A. (Ed.), Phytoplankton Manual. UNESCO, Paris, pp. 33–40. Venrick, E.L., 1978b. How many cells to count? In: Sournia, A. (Ed.), Phytoplankton Manual. UNESCO, Paris, pp. 165–180. Watson, S., McCauley, E., Downing, J., 1997. Patterns in phytoplankton taxonomic composition across temperate lakes of differing nutrient status. Limnol. Oceanog. 42 (3), 487–495. Wehr, J.D., Descy, J.P., 1998. Use of phytoplankton in large river management. J. Phycol 34, 741–749.
Phytoplankton dynamics in a coastal saline lake (SE-Portugal) Pedro Morais *, Maria Alexandra Chícharo, Ana Barbosa Faculdade de Ciências do Mar e do Ambiente, Campus de Gambelas, Universidade do Algarve, 8005-139 Faro, Portugal
Abstract The aim of this study was to characterise phytoplankton dynamics in a coastal saline lake, pinpointing putative biotic and abiotic regulatory variables of its succession and productivity. Between February and September 1998, samples for the analysis of physical, chemical and biological variables were taken fortnightly (except in February and April). The phytoplankton community showed three distinct periods of evolution. The first period (February-March) was characterised by a chroococoid non-colonial cyanobacteria bloom (maximum abundance, 4.3 × 109cells l–1) and also by its decaying. Long water residence and/or nitrogen limitation might have allowed cyanobacteria dominance; while its decaying could be associated to predation by aplastidic nanoflagellates and/or to the beginning of periodical partial renewal of lake water with water proceeding from an adjacent coastal lagoon (Ria Formosa). The second period (April-early August) can be differentiated, from the previous, by reduced abundances of phytoplankton (minimum abundance, 5.7 × 106 cells l–1) and plastidic nanoflagellates dominance. The overall low nutrient concentrations, likely as a consequence of periodical partial water renewal, could explain these results. In the last period (late August-September), increased phytoplankton abundance and the development of a diatom and mixotrophic dinoflagellate bloom was probably the result of a sudden increase in nutrient levels, occurring after a period of intense precipitation. In consequence, primary production reached a maximum value of 1367 mg C m–3 h–1; 36 times higher than a maximum value previously reported for Ria Formosa. © 2003 Éditions scientifiques et médicales Elsevier SAS. All rights reserved. Keywords: Phytoplankton; Succession; Productivity; Bottom-up; Top-down; Saline lake
1. Introduction Once phytoplankton was established as the major primary producer in aquatic environments (Raymont, 1980), one of the main goals of phytoplankton ecology has been the understanding of succession and productivity regulating mechanisms (Pennock and Sharp, 1994). Phytoplankton dynamics can be determined by bottom-up and/or top-down factors (Krebs, 1994). Bottom-up factors control species growth (e.g. light intensity, temperature, salinity, availability of nutrients, its ratios and chemical form), while top-down factors control its biomass (e.g. predation, viral lyses and parasitism) (Donk, 1991; Sherr and Sherr, 1991; Takahashi et al., 1982; Wehr and Descy, 1998). Phytoplanktonic blooms can be a consequence of seasonal processes (Goldman and Horne, 1983), natural (e.g. upwelling) (Moita, 1993) or cultural eutrophication (Hallegraeff, 1995). Cultural eutrophication is defined as the increase * Corresponding author. E-mail address: [email protected] (P. Morais).
© 2003 Éditions scientifiques et médicales Elsevier SAS. All rights reserved. DOI: 1 0 . 1 0 1 6 / S 1 1 4 6 - 6 0 9 X ( 0 3 ) 0 0 0 0 8 - 0
in nutrient concentration in any aquatic ecosystem, resulting in the degradation of its quality, as the outcome of antropic activities (Thompson and Rhee, 1992). The consequences have different intensities according to the available amount of nutrients, the ratios among them and the locality of its reception. The effects of these processes are problematic in confined places and/or with reduced water renewal (e.g. lakes, lagoons, rivers, inland seas) (Ketchum, 1983). In terms of this perspective, this study was undertaken in order to understand the causes that were behind the occurrence of some unpleasant situations, such as fish death and phytoplankton blooms, in the saline lake of Quinta do Lago (south of Portugal). This lake is located in a tourist resort, where some water activities take place. Speculations were made regarding the reason behind these situations, which spilled over the surrounding golf courses fertilisation. So, the objectives of this pioneer work in the saline lake of Quinta do Lago were to characterise, between February and September 1998, the phytoplankton succession and productivity, pinpointing the putative biotic and abiotic variables regulating its development and the evolution of the lake’s trophic state.
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2. Materials and methods 2.1. Study site This study took place in the saline lake of Quinta do Lago (SE-Portugal) (Fig. 1A), which has an area of 6.6 ha, a maximum depth of 2.9 m and an average depth of 2 m. It was carried out from February to September 1998. Fortnightly samples were taken, except in February and April, in three sampling stations (A, B and C) (Fig. 1C). This lake is situated in the west sector of the Ria Formosa Natural Park (Fig. 1B), and was a part of the Ria Formosa lagoon until 1972, when a ditch was built in order to create it. The lake is surrounded in the north by golf courses, in the east and west by houses and in the south by Ria Formosa; from where the water partial renewal for the lake’s water proceeds. Lake water management had two different approaches. Until the end of March 1998, partial water renewal was carried out in a 6-month period, during March and September high tides; afterwards, it was carried out every month, except in August 1998, during high tides. 2.2. Field work methods and laboratory analysis Sampling started between 09:30 and 10:30 h (GMT), except in the first sampling. Station A was the first to be sampled, followed by stations B and C, with a time gap of 45-60 min between each one. After sampling station C, 2 h and 30 min were required to execute the tasks described below. Every studied variable was investigated in each station, except protist abundance, analysed only in station C, the one that has the most complete record. In all the stations, the same sampling procedure was carried out. At every 50 cm depth, vertical profiles of temperature, salinity (probe Microprocessor Conductivity Meter LF196) and photosynthetic active radiation (PAR) (radiometer LI COR LI-1000 Data Logger; 4p sensor SPH Quantum) were made. At 1 m depth,
water samples were taken in a Niskin bottle for chemical and biological analyses. Immediatelyafter sampling, samples for dissolved oxygen concentration and primary production were prepared as meticulously described by Marques (1990). Primary production samples were incubated for 2 h and the method is based on the oxygen method first described by Gaarder and Gran. Oxygen concentrations were determined according to the Winkler method (Grasshoff et al., 1983). The net primary production determined in mg O2m–3 h–1 was converted to mg C m–3 h–1, considering that 1 mg of released oxygen corresponds to 0.313 mg of assimilated carbon (Strickland and Parsons, 1968). The remaining water sample was transferred to recipients with a silicone tube, once this material was established as not being toxic to organisms (Venrick, 1978a). Until sample processing, they were kept in the dark and cooled. On the land, samples for chlorophyll a were filtered through 0.7 µm pore filters (Whatman GF/F); the filtration pressure did not exceed 100 mmHg and the filters were kept frozen (–20 °C) until its spectrofluorimetric analysis (BMEPC, 1988). For the determination of five inorganic macronutrient concentration (ammonium, nitrate, nitrite, orthophosphate and silicate), 20 ml water samples were filtered through 0.45 µm pore cellulose acetate filters (MSI), preserved in 100 µl of saturated HgCl2 solution and were kept refrigerated (4 °C) until spectrophotometric analyses (Kirkwood, 1996), which were conducted according to the protocols of Grasshoff et al. (1983). Protist abundance was determined by applying two different methods. Microplankton abundance was determined with the Utermöhl method (Hasle, 1978), while nanoplankton abundance was determined using the Haas (1982) method. Samples analysed with the Utermöhl method were preserved with acid lugol (6.25% (v/v) final concentration), amplified 400× in a Zeiss IM35 inverted microscope and the cell counts were specified by Venrick (1978b). Samples analysed with the Haas method were preserved with glutaraldehyde 25%
Fig. 1. Geographical location of Quinta do Lago saline lake (A and B) and sampling stations’ spatial disposition (C).
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(2% (v/v) final concentration); stained with proflavin (Fluka), filtered, without exceeding 50 mmHg, through 0.45 µm black polycarbonate filters (MSI) and amplified 1250× in a Leitz DM LB microscope modified for epifluorescence. These two techniques were used because, with the Utermöhl method, autotrophic and heterotrophic taxa cannot be discriminated and others can be under- or over-estimated. With the Utermöhl method, the abundance of diatoms, dinoflagellates and cyanobacteria (except chroococoid forms) were determined, while chroococoid cyanobacteria, Criptophyceae, Prasynophyceae and/or Chlorophyceae abundances were inferred with the Haas method. The observed species were identified, if possible, to species level. The used nomenclature was based on the Tomas (1997) identification manual, but others were consulted (Dodge, 1982; Ricard, 1987; Sournia, 1986; Streble and Krauter, 1973). Autotrophic, mixotrophic and heterotrophic forms of dinoflagellates were established according to several authors (Gaines and Elbrächter, 1987; Lessard and Swift, 1986; Tomas, 1997). Mixotrophic dinoflagellate abundance was included in phytoplankton and phagotrophic protist analysis. 2.3. Meteorological variables Meteorological records concern the Patacão field station (Direcção Regional de Agricultura do Algarve), which is the nearest to the site of study. Atmospheric temperature data are expressed in a 10-d period average, while evaporation (class A evaporometer tub) and precipitation are presented in cumulative values of 10 d.
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Fig. 2. Nutrient limitation according to Si:N and N:P ratios. In each delimited section, nitrogen (N), phosphorus (P) and silica (Si) are ordered by decreased limitation degree.
3. Results The average atmospheric temperature varied between 12.4 °C (20 April) and 25.6 °C (10 August). The minimum atmospheric temperature was 5.5 °C (20 April) and the maximum atmospheric temperature was 34.0 °C (10 August) (Fig. 3A). Cumulative evaporation varied between 14.4 mm (10 February) and 102.3 mm (30 July). On 10 February, the highest cumulative precipitation was registered (80.5 mm); until 20 September, the total cumulative precipitation was scarce (50.5 mm), but in the last decade of September cumulative precipitation reached 65.2 mm (Fig. 3B), coinciding
2.4. Data processing and analysis The extinction coefficient was determined by converting the PAR profile data into logarithm and, according to the least squares method (Snedecor and Cochran, 1989), a linear trend line was adjusted to each profile; the extinction coefficient being the value of the slope. The average intensity of PAR in the mixed layer was determined (Kirk, 1986), taking into account the fact that the mixed layer depth is determined by the thermocline; however, in its absence, it corresponds to sampling station depth. The N:P and Si:N ratios were calculated and plotted on an XY logarithmic graph (Fig. 2), in order to determine the limiting element in the water (Rocha et al., 2002). Each limited area of the graph is expressed by the decreasing order of the limiting element. The trophic State Index related with chlorophyll a concentration (TSI (Chl a)), was used in order to examine the evolution of the lake’s trophic state (Carlson, 1977). TSI ranges between 0 and 100, varying from oligotrophic to hypereutrophic conditions (Carlson et al.). The main meteorological, physical, chemical and biological variables were inter-correlated with Spearman R non-parametric test. Bonferroni correction was applied to the chosen significance level (P < 0.05) to reduce the probability of significant casual correlations (Snedecor and Cochran, 1989).
Fig. 3. Maximum, average and minimum atmospheric temperature (A), evaporation and precipitation (B) registered in Patacão meteorological field station.
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Fig. 5. Temporal evolution of extinction coefficient (A) and average intensity of PAR in the mixed layer (B) in each of the three stations sampled. The arrows on top of graph A represent the moments of the lake’s water partial renewal. Fig. 4. Vertical profiles of temperature (A) and salinity (B) in each station.
with the beginning of a mixotrophic dinoflagellate and diatom bloom (Fig. 11). The water temperature oscillated between 17.6 °C (18 February) and 28.5 °C (21 August) (Fig. 4A). Salinity increased from 18 February (21.1) to 7 September (42.4) and had a decreased superior to 1 between 7 and 30 September (Fig. 4B). The entire vertical profile data show an absence of water column stratification (Fig. 4A, B). The extinction coefficient varied between 0.22 m–1(13 May) and 3.44 m–1 (30 September) (Fig. 5A), which coincided, respectively, with the minimum chlorophyll a concentration (Fig. 10) and the mixotrophic dinoflagellate and diatom bloom (Fig. 11). The average intensity of PAR in the mixed layer was between 87.8 µmol PAR s–1 m–2 (30 de September) and 1396.6 µmol PAR s–1 m–2 (22 April) (Fig. 5B). The dissolved oxygen concentration in the water varied from 1.66 ± 0.02 mg O2l–1 (7 September) to 9.77 ± 0.01 mg O2 l–1 (18 February). The similarity between stations was high, except in the last sampling (Fig. 6). Nutrient concentrations were, generally, less than 1 µM, apart from silicate concentrations which varied from 1.20 ± 0.09 to 17.68 ± 0.29 µM. At times, nitrate and orthophosphate
Fig. 6. Temporal evolution of dissolved oxygen concentration in each of the three stations sampled. The arrows on top of the graph represent the moments of the lake’s water partial renewal.
concentrations were slightly higher than 1 µM. Ammonium and nitrite concentrations were always less than 0.440 µM (Fig. 7A-E). If nutrients were limiting for phytoplankton growth, then Nitrogen (N) would have been the most limiting (Fig. 8). Phagotrophic protist abundance varied from 0.32 × 106cells l–1 (8 July) to 12.7 × 106 cells l–1 (30 September) (Fig. 9A). On 30 September, all phagotrophic protist groups presented its maximum abundances, except heterotrophic
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Prorocentrum minimum, a mixotrophic dinoflagellate, account for 62.5% (Fig. 9). Chlorophyll a concentration varied between 0.70 ± 0.00 µg Chl a l–1 (13 May) and 49.37 ± 2.00 µg Chl a l–1 (30 September). Generally, from 22 April to 21 August, the average concentration was less than 6 µg Chl a l–1. From 6 August to 30 September, chlorophyll a concentration increased 32.8 times (Fig. 10). The highest phytoplankton abundances were registered in late winter/early spring and in late summer/early autumn, while the lowest were found in between. Its abundance oscillated between 5.7 × 106cells l–1 (8 July) and 4.3 × 109 cells l–1 (18 February). From 18 February to 8 July, phytoplankton abundance decreased progressively, but between 11 and 25 March, a striking decrease was noticed, from 2.0 × 109 to 51.1 × 106 cells l–1. After 8 July, an increase in phytoplankton abundance was noticed until 30 September, when a relative maximum was registered (104.1 × 106 cells l–1) (Fig. 11A). From 18 February to 11 March, the phytoplanktonic community was dominated by chroococoid cyanobacteria, representing, respectively, 97.4 and 90.8%. After, and until the end of the study, autotrophic nanoflagellates were the most representative group, usually with relative frequencies greater than 98%. However, on 30 September, diatoms and mixotrophic dinoflagellates represented, respectively, 30.7 and 20.3% of the community, while autotrophic nanoflagellates represented 47.9% (Fig. 11B). The primary production variability between station was reduced, except on 30 September, when a maximum value of 1367.4 mg C m–3h–1 was registered (Fig. 12). TSI (Chl a) index varied from 7.1 ± 0.0 (13 May) to 68.9 ± 0.4 (30 September), which corresponds to oligotrophic and hypereutrophic levels (Fig. 13), following the evolution pattern presented by phytoplankton abundance (Fig. 11A). Spearman R correlation matrix (Table 1) shows significant correlations among some meteorological variables, namely water temperature, salinity, atmospheric temperature and evaporation. Dissolved oxygen in the water and mixotrophic dinoflagellates are significantly correlated, as aplastidic flagellates and autotrophic nanoflagellates. The highest correlations with primary production were obtained with temperature, nitrites and orthophosphates. 4. Discussion
Fig. 7. Temporal variations of ammonium (A), nitrite (B), nitrate (C), orthophosphate (D) and silicate (E) concentration in each of the three stations sampled. The arrows on top of graph A represent the moments of the lake’s water partial renewal.
dinoflagellates. Aplastidic flagellates were the most representative group of phagotrophic protists, with relative frequencies greater than 68.6%, except on 30 September when
In temperate lakes, the phytoplanktonic community is submitted to strong seasonal variations of biotic and abiotic variables. Thus, this community responds to those variations by presenting a different species composition, proportion and abundance. Usually, during spring, the community is dominated by diatoms; in summer, small flagellates and cyanobacteria have maximum abundances; through autumn and winter, the community is dominated by diatoms, dinoflagellates and cyanobacteria (Goldman and Horne, 1983); however, in Quinta do Lago temperate saline lake, this successional pattern was not verified.
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Fig. 8. Assessment of N, P or Si limitation in each sampling station. Note: Station A, data corresponding to 11 March and 6 August are not represented; Station B, data corresponding to 11 March, 13 May and 6 August are not represented; Station C, data corresponding to 22 April are not represented.
The reduced spatial variability of phytoplankton physiological variables and physical and chemical water variables, plus the absence of water column stratification, evokes the idea that there is only one water mass that allows the existence of only one phytoplanktonic population (Anderson et al., 1994). Phytoplankton dynamics presented three distinct periods, which can be inferred by the analyses of its abundance and composition, chlorophyll a concentration and the lake’s trophic state evolution. The first period (18 February-25 March) was characterised by long water residence, hypereutrophic and eutrophic trophic levels, the dominance of non-colonial chroococoid cyanobacteria bloom, and by its collapse and transition to autotrophic nanoflagellates dominance. In line with the bibliography (Hickel, 1985; Klemer and Barko, 1991; Meyer, 1994; Paerl, 1996), these cyanobacteria blooms usually occur in eutrophic and hypereutrophic aquatic systems, with periods of long water residence, months or even years. Long water residence in the lake, since September 1997, might explain the persistence of chroococoid cyanobacteria bloom, while its collapse could be related to the enhancement of the lake’s water partial renewal at the end of March 1998. Bloom collapse can also be related to top-down control (Goldman and Horne, 1983), maybe due to the maintenance of high and regular abundance of aplastidic flagellates, which are important consumers of cyanobacteria (Sherr and Sherr, 1991).
In the second period (22 April-6 August), the lake was subjected to mensal partial water renewal; the phytoplanktonic community was clearly dominated by autotrophic nanoflagellates and the lake’s trophic state oscillated between oligotrophic and mesotrophic. In lakes under oligotrophic conditions, phytoplanktonic species have reduced dimensions (Watson et al., 1997), so their high surface/volume ratio allows them to compete more efficiently for available nutrients than species of higher dimension, and therefore, to dominate the community (Anderson et al., 1994; Sommer, 1991). Predation losses are difficult to evaluate; once it could be reduced, due to low predatory population (Watson et al., 1997), or high when sustained by fast nanoplankton growth. Mensal partial water renewal might have influenced the maintenance of a certain species composition in the lake; once, during that period in Ria Formosa, the community was also dominated by autotrophic flagellates (Chícharo et al., 2000). However, phytoplankton abundance in the lake was always higher, probably due to more stable conditions in the lake, allied with optimal physical characteristics (Therriault, 1990), to higher predation rates in the lagoon, and perhaps because Ria Formosa nanoplankton was estimated only with the Utermöhl method, which might underestimate the lower fraction of plankton. During the last period (21 August-30 September), the increase in the lake’s trophic state to hypereutrophic condi-
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–1
Fig. 9. Evolution of total phagotrophic protist abundance (cells l ) (A) and relative frequency of each phagotrophic protist group (B). The arrows on top of graph A represent the moments of the lake’s water partial renewal.
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Fig. 11. Evolution of total phytoplankton abundance (cells l-1) (A) and relative frequency of each phytoplanktonic group (B). The arrows on top of graph A represent the moments of the lake’s water partial renewal.
tions, matched with the bloom of diatoms and mixotrophic dinoflagellates (P. minimum) and with high precipitation. It is important to state that during 1 month and 15 d, from late July to early September, the lake’s water partial renewal was not carried out. Until 7 September, the increase in waters residence, in addition to stable and optimal water temperatures, might lead to the increase in phytoplankton abundance and the lake’s trophic state. The subsequent water partial
renewal was not efficient once a phytoplanktonic bloom developed, probably as a result of intense precipitation. Severe eutrophication events are supposed to occur during late summer and early autumn (Strain and Yeats, 1999), usually as a consequence of high precipitation followed by periods of high insulation (Hickel, 1988). Primary production is also positively influenced by this conjecture (Paerl et al., 1999), perhaps as a result of introduced nutrients in the lake, which proceed from its drainage area. On 30 September, consider-
Fig. 10. Evolution of chlorophyll a concentration in each of the three stations sampled. The arrows on top of the graph represent the moments of the lake’s water partial renewal.
Fig. 12. Evolution of primary production in each of the three stations sampled. The arrows on top of the graphs represent the moments of the lake’s water partial renewal.
S94 Table 1 Spearman R correlation (P < 0.002) based on the most important variables obtained. The underlined correlations are significant for a significance level less than 0.002. ANF, autotrophic nanoflagellates; °C atm, atmospheric temperature; °C wat, water temperature; Chl a, chlorophyll a concentration; Cyano, cyanobacteria; Cili, ciliates; Crip, Criptophyceae; Diat, diatoms; DinA, autotrophic dinoflagellates; DinH, heterotrophic dinoflagellates; DinM, mixotrophic dinoflagellates; Evap, evaporation; FA, aplastidic flagellates; Im, average PAR intensity in the mixed layer; Ke, extinction coefficient; NH4+, ammonium; NO2–, nitrites; NO3–, nitrates; O2, dissolved oxygen; PO43–, orthophosphates; PP, primary production; Pra/Clo, Prasinophyceae and or Chlorophyceae; Prec, precipitation; Sal, salinity; SiO44–, silicates Sal
1 0.841 0.786 –0.269 0.407 –0.056 –0.566 0.538 –0.462 0.070 0.476 0.530 0.632 0.260 –0.390 –0.393 0.710 –0.531 –0.094 0.016 0.339 0.143 –0.275 0.066
°C atm
1 0.890 –0.354 0.104 0.245 –0.538 0.601 –0.429 0.252 0.564 0.568 0.484 0.154 –0.505 –0.531 0.564 –0.580 –0.050 –0.253 0.096 –0.160 –0.168 0.011
NH4+ NO3–
Evap
Prec
Ke
Im
O2
PP
1 –0.435 –0.049 0.503 –0.621 0.385 –0.610 0.154 0.597 0.441 0.258 –0.133 –0.742 –0.765 0.393 –0.605 –0.050 –0.302 0.303 –0.091 –0.374 –0.133
1 0.119 0.017 0.608 0.196 0.169 0.175 0.020 –0.217 –0.110 –0.273 0.232 0.511 –0.169 0.643 –0.080 0.558 0.327 0.154 0.116 0.249
1 –0.601 0.115 0.483 0.049 –0.273 –0.220 0.218 0.176 0.540 0.484 0.366 0.294 –0.019 0.055 0.731 0.008 0.124 0.132 0.448
1 –0.203 –0.018 –0.280 0.227 0.158 –0.035 –0.273 –0.625 –0.671 –0.750 –0.273 –0.203 0.309 –0.364 0.035 –0.551 –0280 –0.331
1 0.070 0.445 –0.140 –0.217 –0.204 –0.341 0.281 0.665 0.671 –0.349 0.825 –0.160 0.451 –0.039 0.091 0.523 0.470
1 0.042 1 0.073 –0.469 0.462 –0.242 0.457 0.069 0.287 –0.055 0.333 0.411 –0.049 0.610 –0.049 0.443 0.637 –0.019 0.070 0.635 0.067 0.011 0.2940.330 –0.238 –0.077 –0.488 0.056 –0.074 0.431 0.459 0.210 0.227
1 0.364 –0.436 0.378 –0.311 –0.343 –0.035 –0.350 –0.238 –0.130 –0.165 0.330 0.340 –0.536 –0.303
NO2–
PO43– SiO44– Chl a
ANF
FA
DinA
DinM DinH
Diat
Pra/Clo Crip
1 0.463 0.338 –0.021 –0.644 –0.306 0.355 0.050 –0.379 0.047 0.501 0.357 –0.237 –0.089
1 0.334 0.391 –0.163 –0.235 0.659 –0.030 0.044 –0.148 0.061 –0.336 0.192 0.336
1 0.801 –0.149 0.465 –0.061 0.498 –0.369 –0.003 0.492 0.541
1 –0.163 0.598 –0.414 –0.094 –0.039 0.377 0.253 0.387
1 –0.193 0.072 0.503 –0.048 0.044 0.281 –0.019
1 –0.300 –0.149 0.138 0.269 0.391 0.398
0.267 0.218 0.030 0.597
1 0.535 1 –0.570 –0.323 1 0.238 –0.078 0.288 1
1 0.323 –0.055 0.044 0.580 –0.297 –0.180 0.239 0.105 0.262 –0.226 –0.099
1 0.625 0.322 0.361 0.139 –0.262 0.505 –0.204 0.079 0.578 0.640
Ciano Cili
P. Morais et al. / Acta Oecologica 24 (2003) S87–S96
°C Ág °C Ág 1 Sal 0.853 °C atm 0.900 Evap 0.938 Prec –0.463 Ke 0.074 Im 0.357 –0.655 O2 PP 0.462 NH4+ –0.649 NO3– 0.259 NO2– 0.470 PO43– 0.319 SiO44– 0.424 Chl a –0.046 ANF –0.641 FA –0.689 DinA 0.482 DinM –0.741 DinH 0.059 Diat –0.344 Pra/Clo 0.171 Crip –0.037 Ciano –0.315 Cili –0.235
1 1 –0.529 –0.654 0.398 –0.250
P. Morais et al. / Acta Oecologica 24 (2003) S87–S96
Fig. 13. Evolution of Trophic State Index relative to chlorophyll a concentration in each of the three stations sampled. The arrows on top of the graph represent the moments of the lake’s water partial renewal.
able spatial differences were found in dissolved oxygen concentration and primary production; probably a consequence of high photosynthetic rate plus the time gap between sampling each station. Primary production has a positive correlation with nutrient availability (Raymont, 1980), however, in cases of nutrients saturation, temperature and light intensity are the key factors (Anderson et al., 1994), although light intensity could play a more important role (Raymont, 1980). The average intensity of PAR in the mixed layer did not explain primary production variation, so photoinhibition over phytoplankton growth might have occurred, once optimal values were not verified, since they were almost always greater than 300 µmol PAR s–1m–2 (Raymont, 1980). In Ria Formosa, the maximum reported primary production was 38.3 mg C m–3 h–1 (Falcão and Vale,1992), which is 36 times lower than the maximum found in the lake.
5. Conclusions In the saline lake of Quinta do Lago, physical, chemical and biological variables presented reduced variability and similar evolution, which suggests the existence of one water mass and one phytoplanktonic population in the lake. For these reasons, sampling in a central position could be considered in future studies. The increase in water temperature might have allowed phytoplankton to optimise its growth and productivity. However, high light intensity in the water column might have counteracted temperature increment effect over primary production by a process of photoinhibition. Nitrogen limitation might have been important in defining of phytoplankton communities, mainly during non-colonial chroococoid cyanobacteria dominance. A possible decrease in nutrient concentration, in relation with the period prior to the beginning of the study; predation of aplastidic flagellates on those cyanobacteria and water partial renewal were possi-
S95
bly in the origin of the bloom collapse. Afterwards, mensal water partial renewal and reduced nutrient concentration seemed to propitiate autotrophic flagellates the required conditions to dominate the phytoplanktonic community. At the end of the study, a possible entrance of nutrients into the lake, probably by runoff waters as a consequence of high precipitation, might have triggered the conditions for the development of the diatom and mixotrophic dinoflagellate bloom. Partial water renewal of lake water was probably important in defining a phytoplanktonic community similar to the one found in the western part of the Ria Formosa and in defining the lake’s trophic state evolution, mainly in its reduction and maintenance. However, partial water renewal was not efficient, in sustaining reduced trophic levels and in defining the structure of phytoplankton community, when intense precipitation matched with periods of high temperature and insolation.
Acknowledgements The authors would like to acknowledge Dr. Helena Marques, Mr. Fernando Braga and Mr. Artur for their helpful contribution during field work and especially to Ms. Ana Marques for her involvement during manuscript development.
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