Influence of Hydrology on Phytoplankton Species Composition and ...

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sulcata, M. moniliformis var. octogona, Cylindrotheca closterium, Euglena sp. 1, and Chroomonas sp. 1), indicating no association with the abiotic gradients,.


Vol. 28, No. 6, p. 884–895

December 2005

Influence of Hydrology on Phytoplankton Species Composition and Life Strategies in a Subtropical Coastal Lagoon Periodically Connected with the Atlantic Ocean SYLVIA BONILLA*, DANIEL CONDE, LUIS AUBRIOT, and MARI´A



Seccio´n Limnologı´a, Facultad de Ciencias, Universidad de la Repu´blica Igua´ 4225, 11400-Montevideo, Uruguay ABSTRACT: A survey was carried out to investigate the relationship of phytoplankton biovolume, structure, and species life strategies with major abiotic factors in a subtropical choked coastal lagoon (34u339S, 54u229W) naturally connecting with the Atlantic Ocean several times a year. Marine and limnetic influence areas were sampled on a monthly basis during two periods, one of low rainfall and high conductivity (August 1996 to February 1998) and a second period with the opposite tendency (December 1998 to March 2000). Photosynthetically active radiation availability was high and reached the bottom (.1% of the incident light), while dissolved inorganic nitrogen (0.6–18.4 mM), soluble reactive phosphorus (,0.3–2.7 mM), and reactive silica (5–386 mM) were highly variable. Life strategies were identified in the phytoplankton as a function of morphology. Cstrategists, invasive planktonic and epipelic species of small size, and R-strategists, mixing-dependent species of medium size, characterized this permanently mixed system. High frequency of exchange with the ocean prevented high biomass accumulation. Phytoplankton biomass was lower in the second period of high rainfall (2.3 and 1.1 mm3 l2l for period 1 and 2, respectively). A canonical correspondence analysis showed that conductivity, nitrogen, phosphorus, and silica were the main environmental variables explaining phytoplankton species composition patterns. During the first period, Bacillariophyceae (mostly pennate species) and the potentially toxic Prorocentrum minimum were dominant; during the second period a higher contribution of flagellates (Cryptophyceae, Euglenophyceae, Prasinophyceae, and flagellates ,7 mm) was found. Differences of phytoplankton biomass, main taxonomic groups, and strategies were found between periods but not between limnic and marine areas, suggesting that hydrological dynamic is more relevant than seasonal and spatial differences.

During long periods of isolation from the sea, lagoons behave as shallow lakes and the internal biogeochemical processes become more important, allowing the development of phytoplanktonic species of high biovolume and low growth rates, which may develop blooms (Melo 2001). Due to large temporal and spatial variability and the absence of ecological models, phytoplankton dynamics in these systems are still poorly understood. Physiology, growth, and abiotic requirements of phytoplankton species reflect their polyphyletic origin (Margalef 1978; Tilman et al. 1986; Reynolds 1991). Traditionally, predictive models of phytoplankton dynamics consider the community at the level of main phylogenetic groups (Divisions or Classes). Based on Grime’s Competitors, Stresstolerants and Ruderals (CSR) triangle model for terrestrial plants, Reynolds (1984, 1991) identified three primary strategies among phytoplankton species, based on the assumption that morphometric characteristics of species reflect their physiological responses and life strategies. C-species are invasive colonists (instead of competitors as in the model of Grime) that exploit the plentiful resource conditions of light and nutrients (e.g., Synechococcus sp., Chlorella sp., small diatoms). S-species tolerate

Introduction Coastal lagoons are unique systems, typically characterized by bidirectional horizontal flows, permanent mixing of the water column, and abrupt changes in residence time and water depth. Particularly interesting are choked lagoons, separated from the ocean by a sand bar that naturally opens through a channel, depending on the local rainfall regime (Day and Yan ˜ ez-Arancibia 1982; Knoppers 1994; Duarte et al. 2002). In these systems, periodical hydrological events like floods and marine intrusions cause large temporal and spatial variations in phytoplankton composition and production, due to the replacement of species and changes in conductivity, nutrients, and light availability (Comı´n and Valiela 1993; Kjerfve 1994; Suzuki et al. 1998; Kormas et al. 2001; Medina-Go´mez and Herrera-Silveira 2003). Accumulation of phytoplankton biomass can also depend on hydrology. For example, water discharge into the coastal area can wash out phytoplankton biomass, preventing the development of blooms (Suzuki et al. 1998, 2002; Moreira-Turcq 2000). * Corresponding author; tele: 5982-5258618, ext. 148; fax: 59825258617; e-mail: [email protected] ß 2005 Estuarine Research Federation


Phytoplankton of a Subtropical Coastal Lagoon

resource depletion (e.g., Microcystis aeruginosa, Ceratium sp., Volvox aureus), and ruderals (R-species) overcome frequent or continuous entrainment beyond the photic zone, which determines a high frequency of intermittency in the supportive capacity (e.g., most of the diatoms). C-strategists exhibit rapid nutrient uptake, assimilation, and growth rates (.0.8 d21), while at the other extreme Sstrategists present complex mechanisms of perennation, slow growth (,0.9 d21), and persistency under less suitable environmental conditions (Reynolds 1991). In coastal lagoons, large and highly frequent changes in the physical conditions and continuous water column mixing may favor the development of C- and R-strategists. Long-term isolation from the sea, stable conditions, and nutrient stress could trigger the dominance of S-strategists. The southeastern coast of South America contains several coastal lagoons of ecological and economic relevance, but they have been poorly studied (Seeliger et al. 1997). These systems exhibit periodic marine intrusions, but the natural hydrology is artificially modified in some cases, threatening their natural functioning (Odebrecht and Abreu 1997). Laguna de Rocha is located on the Atlantic coast of Uruguay and connects with the ocean after the natural (and occasionally artificial) opening of its sand bar, 2 to 6 times per year (Pintos et al. 1991). The precipitation pattern in its basin regulates the frequency and amplitude of the connection. It is possible to identify an abiotic temporal gradient from limnetic to brackish phases, as well as spatial differentiation between a marineinfluenced area with higher conductivity and a limnetic zone with higher nutrient concentration, light attenuation, and primary production (Pintos et al. 1991; Conde et al. 2000, 2002). We expect the hydrological behavior of Laguna de Rocha to be the major factor explaining phytoplankton composition and dynamics. We hypothesize that phytoplankton composition and biomass is significantly different between limnetic and marine areas and between periods of high and low marine influence. To assess this hypothesis, two different hydrological periods were compared. The first one was dominated by precipitation below the historical average and high conductivity (August 1986 to February 1998), while the second one was dominated by rainfall above the historic average and low conductivity, followed by a drought period (December 1998 to March 2000). We explored the abiotic factors that may explain the phytoplankton species and biovolume variability during both periods. We also hypothesized that phytoplankton of Laguna de Rocha is dominated by C- and Rstrategists. The morphological-functional approach


Fig. 1. Location of the sampling sites in Laguna de Rocha. North (N) and South (S) sampling sites are indicated with black circles. Littoral marshes in the northern areas (in gray), main isobaths, and the connection to with the Atlantic Ocean through the sand bar (black arrow) are also shown.

to identify species strategies in the phytoplankton community was used. STUDY SITE Laguna de Rocha (34u339S, 54u229W; mean depth 5 0.5 m, surface area 5 72 km2, watershed area 5 1,312 km2) is included in a MaB/UNESCO Biosphere Reserve. The climate of the region is subtropical (Bailey 1998; historical annual air temperature for 1951–1991 5 16.0uC), with rainfall well distributed throughout the year (historical annual rainfall for 1951–1991 5 1,105 mm). The northern zone of the lagoon presents marshes of Schoenoplectus californicus as well as areas covered by submerged Potamogeton sp. and Myriophyllum sp. (Rodriguez-Gallego personal communication; Fig. 1). Sandy-silty and sandy sediments characterize the North and South areas, respectively (Sommaruga and Conde 1990). The lagoon, located on a microtidal coast, periodically connects with the Atlantic Ocean through a narrow channel that opens naturally on the sand bar, depending on lagoon water level and sea wave action (Conde et al. 2000). Occasionally,


S. Bonilla et al.

the sand bar is also opened artificially. The connection with the ocean occurs when the inner water level of the lagoon reaches 1.3 m depth, producing a mean water discharge of 570 m3 s21 with a current flow of 2.1 m s21. The marine intrusion takes place in the South area and its durability depends on the width of the channel (15– 200 m), which usually lasts between 5 and 100 d (Conde and Sommaruga 1999). The spatial influence of the marine intrusion towards the North depends on the occurrence of strong long lasting southern winds. The hydrological dynamics of Laguna de Rocha can be described by a cycle of three phases that occur several times per year that are accompanied by significant shifts in water transparency (Conde et al. 2000). During the first phase, characterized by dominance of freshwater discharge, most of the lagoon exhibits homogeneous optical characteristics, and high loads of dissolved and particulate organic substances. This phase lasts when the increase of water level leads to the opening of the sand bar. After the subsequent freshwater discharge, the ocean intrudes into the lagoon (Phase II), usually under the influence of southeastern winds. While salinity gradient progressively develops, the southern area of the lagoon shifts to a brackish condition while the northern zone remains limnic for a longer period. Southeastern winds lasting for several days can move saline waters further North (Phase III) increasing the differences between marine (transparent, poor nutrient content) and limnic extremes (turbid, nutrient enriched). Aerial views of the closed and open situations can be viewed at The water column is well mixed, oxygenated, and turbid due to its shallowness and the resuspension of fine sediments (Conde et al. 1999). A human population of ca. 30,000 inhabitants is located in the Laguna de Rocha basin, where main land uses are extensive cattle farms, forestation, and artisanal fisheries (Conde and Sommaruga 1999). There is still no clear evidence of human effects on the water quality of the lagoon (Conde and Sommaruga 1999). Material and Methods ABIOTIC VARIABLES Two sampling stations were located at the lagoon corresponding to the freshwater (North) and marine (South) influence areas. South (S) and North (N) sampling stations were located at 1 and 15 km from the sand bar, respectively (Fig. 1). The study was performed on a monthly basis during the two periods mentioned above.

During each sampling, water depth (Z), temperature (T; Horiba OM-14), dissolved oxygen (DO, Horiba OM-14), photosynthetically active radiation profiles (PAR, measured every 5 cm with a Li-Cor LI250/2p collector), pH, and conductivity (K, Horiba ES-12) were registered in situ at both stations (N and S). PAR diffuse attenuation coefficient K d (m21) was calculated following Kirk (1994). Since the water column was permanently mixed, subsurface water samples were taken with a Van Dorn type sampler. Analysis of dissolved inorganic nitrogen (DIN; ammonium + nitrite + nitrate), soluble reactive phosphorus (SRP), reactive silicate (RS), suspended solids (SS), total nitrogen (TN), and total phosphorus (TP) were performed according to APHA (1995) and Valderrama (1981). Daily rainfall and hourly wind intensity data were obtained from the National Meteorological Service (Rocha Station). For correlations with biological data, accumulated rainfall (pr) between samplings was calculated. Standardize values (standard deviation units) were calculated for rainfalls, as the monthly average minus the average for that month over historical monthly rainfall average (1951– 1991). As a consequence, zero indicates the mean value and no deviation from historical tendency, positive values are higher than historical average, and negative values are lower than historical average. PHYTOPLANKTON Subsurface samples were collected at both stations and concentrated by sedimentation for taxonomic identification. Subsamples were kept fresh until analyses, while others were fixed to a final concentration of Na2CO3-neutralized 5% formaldehyde solution. Fixed subsamples were oxidized with 50% H2O2 for diatom identification (Battarbee 1986) and analyzed under optic Olympus and scanning electronic (Jeol JSM-5200) microscopes. Duplicate subsurface samples of 350 ml were taken and fixed with Lugol solution for quantitative analyses. Duplicate microalgae counting were done by transects until obtaining 400 units (cells or colonies) according to Utermo¨hl (1958), using a Nikon Diaphot inverted microscope (400 X) with phase contrast. The cell biovolume and surface area were calculated based on geometric shapes and the average of the microscopic dimensions of 10–30 organisms per taxon (Hillebrand et al. 1999). The classification system of van Den Hoeck et al. (1995) was followed for Classes and Divisions. Krammer and Lange-Bertalot (1986, 1988, 1991), Tomas (1997), and Round et al. (1992) were used as main taxonomic references for genera and species. The model of three strategies, invasives (Cstrategists), ruderals (R-strategists), and stress toler-

Phytoplankton of a Subtropical Coastal Lagoon


Fig. 2. Monthly average standard deviation units for rainfall for periods 1 and 2.

ants (S-strategists) developed by Reynolds (1991) was applied to the most representative taxa (.25% of total biovolume). Based on morphometric variables (specific biovolume, maximal linear dimension: MLD, and surface: volume ratio: S:V), the life strategies of main taxa were identified for Laguna de Rocha. C-species are characterized by small cell volume (,5 3 103 mm3), high S:V ratio (.0.3 mm21), and short MLD (,80 mm). S-species are large cells, colonies, or filaments (.104 mm3), and show low S:V ratios (,0.3 mm21) and high MLD (up to 500 mm). R-species maintain high S:V ratios (.0.3 mm21), intermediate size (500–105 mm3), and MLD (10–300 mm; Reynolds 1991). DATA ANALYSES To test differences between stations and periods based on abiotic variables, total phytoplankton abundance, total biovolume, main taxonomic (Classes) groups, and life strategies, the nonparametric Kruskal-Wallis (K-W) test was used because data were not distributed normally after simple transformations. To evaluate the correlation between pairs of variables, the nonparametric Kendall correlation was used (K Tau). To explore the principal patterns of the phytoplankton distribution and their relation with the environmental variables, we selected the canonical correspondence analysis (CCA) because of the unimodal distribution of the data (ter Braak and Smilauer 1998). For this analysis, the biovolume of those species equal or above 25% of the total biovolume were used and the Bray-Curtis similarity index was applied on transformed data (ln x + 1). For abiotic data (pr, T, DO, K, Z, pH, RS, DIN, SRP, and SS), a distance matrix was calculated on standardized values (x 2 average/standard deviation). The significance (p , 0.05) of the environmental

Fig. 3. Temporal variation of conductivity in South (black circles) and North (white circles) stations (top); vertical gray areas indicate periods of closed sand bar. Temporal variation of water temperature at both stations (bottom); symbols as in the top plot.

variables to explain the variance of species was tested with the Monte Carlo permutation test (199 unrestricted permutations) for the first axis and all axes (null hypothesis: the species data are unrelated to the environmental data). This permutation test is an analysis for testing the statistical significance obtained by repeatedly permuting the samples. Unrestricted permutations are appropriate for completely randomized designs like our case. The number of 199 permutations selected was a compromise between the maximum power of the test and time spent. Correlations between the environmental variables and the axes were also performed (ter Braak and Smilauer 1998). All statistical analyses were run with Statistica and CANOCO 4.0. Results ENVIRONMENTAL AND WATER VARIABLES During the first period, Laguna de Rocha basin was dominated by lower monthly precipitation (below the historical average; 28.9–168.8 mm) compared to the second one (above the historic average; 33.3–357.3 mm; Fig. 2). The lagoon connected eight times with the ocean during the first period, while only four connections were registered during the second one (Fig. 3). For the whole study,


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TABLE 1. Average (6 SD) of the abiotic variables for the study period (1996–2000) at stations South (S) and North (N) during periods 1 and 2, respectively. Temperature (T), extinction coefficient (K d), surface PAR (PARsurf), bottom PAR (PARbot), mixing zone-euphotic zone ratio (Zmix:Zeu), depth (Z), conductivity (K), dissolved oxygen (DO), pH, total suspended solids (SS), suspended organic matter (OM), dissolved inorganic nitrogen (DIN), soluble reactive phosphorus (SRP), reactive silica (RS), total nitrogen (TN), and total phosphorus (TP); n 5 53, except in K d n 5 40. S1

T (uC) Kd (m21) PARsurf (mmol m22 s21) PARbot (mmol m22 s21) Zmix:Zeu Z (m) K (mS cm21) DO (mg l21) pH SS (mg l21) OM (%) DIN (mM) SRP (mM) RS (mM) TN (mM) TP (mM)

17.5 1.7 834.5 315.9 0.22 0.8 24.1 9.1 7.9 20.5 36.4 7.7 0.6 31.7 44.8 2.4

(4.6) (0.9) (657.2) (280.4) (0.13) (0.3) (13.7) (1.1) (0.4) (21.6) (31.5) (4.6) (0.4) (35.8) (36.5) (1.9)

water depth varied ca. 1 m (0.20–1.40 m) and it was significantly correlated with pr (Tau 5 0.336, p , 0.001). Weak southwestern and northern winds (average: 2.90 km h21) prevailed during samplings, with a maximum speed of 14.1 km h21 (April 25, 1997). The minimum water temperature during samplings was observed in August 1997 at station S (8.6uC) and the maximum in January 2000 at station N (29.3uC). According to the temperature profiles (data not shown) the water column was permanently mixed, so the mixing zone (Zmix) involved the complete water column. Average surface PAR was similar at both stations (average for entire study period: 1,033 and 1,327 mmol m22 s21 for station S and N, respectively; Table 1). Bottom PAR represented from ca. 12% to 88% at station S and from 1% to 56% at station N of the surface PAR (minimum 5 15 mmol m22 s21 at station N; maximum 5 990 mmol m 22 s 21 at station S). The theoretical euphotic zone (Zeu) was always deeper than Z. The Zmix:Zeu ratio was low (#1) indicating high light availability for the algae, although the ratio increased from station S period 1 to station N period 2 (Table 1). The highest value (Zmix:Zeu 5 2.80) was registered in station N on June 30, 1999. Suspended solids (K-W, H 5 5.684, p , 0.05) and K d (K-W, H 5 11.791, p , 0.0001) were significantly higher at station N than at station S, and the K d was positively correlated with SS at both stations (N: Tau 5 0.389, p , 0.05; S: Tau 5 0.491, p , 0.001). A wide range of conductivity was found, varying from limnetic waters at station N (minimum 5 0.064 mS cm21, equivalent to 0.04 psu) to brackish waters at station S (maximum 5 48.90 mS cm21, equivalent to 31.30 psu; Fig. 3). Significant differences in conductivity were found between sampling


18.9 3.1 1216.8 726.5 0.53 0.9 15.0 9.7 7.9 30.2 25.1 4.0 1.0 100.9 45.6 2.7

(4.9) (2.1) (562.1) (372.6) (0.42) (0.4) (8.4) (1.4) (0.3) (23.4) (7.8) (3.8) (0.7) (49.2) (22.1) (1.3)


19.4 3.4 1198.2 185.1 0.45 0.7 6.7 8.1 7.7 35.9 41.0 7.0 1.1 124.8 53.9 4.17

(3.9) (1.5) (726.3) (200.7) (0.25) (0.2) (8.0) (1.6) (0.5) (17.9) (54.0) (3.4) (0.6) (96.5) (32.1) (3.6)


20.6 3.8 1492.5 262.5 0.83 0.8 3.2 9.1 7.7 38.5 24.1 6.1 1.1 161.5 52.6 3.3

(5.2) (1.9) (372.0) (23.3) (0.78) (0.5) (3.9) (1.7) (0.6) (20.2) (7.6) (4.4) (0.4) (78.1) (27.1) (1.7)

stations (K-W, H 5 24.289, p , 0.0001). Higher conductivity values were observed during the first period and at the end of the second period (February and March 2000; Table 1). pH varied from slightly acidic to alkaline (6.45–8.53) and DO indicated oversaturation (Table 1). The water column was always well oxygenated and significantly higher values of DO were found during the second period (K-W, H 5 5.643, p , 0.05). The concentration of DIN, SRP, and RS varied widely along the study. While RS concentration was always high (range: 5.0–385.7 mM) and SRP ranged from low (0.1 at station S on May 5, 1997) to high values in some cases (2.5 mM at station N on December 12, 1996 and 2.7 mM at station S on January 13, 2000), DIN was always low (0.6– 18.4 mM). When RS was compared among sites and periods, significantly higher values were found at station N (K-W, H 5 10.029, p , 0.005) and during the second period (K-W, H 5 14.906, p , 0.00l; Table 1). At station S, RS was negatively correlated with conductivity (Tau 5 20.304, p , 0.02). The DIN:SRP ratio reached higher values during the first period (8.3 and 12.7, average for station S and N, respectively) than during the second one (6.0 and 4.3, average for station S and N, respectively). The concentration of TN and TP were similar (p . 0.05) between stations and periods (Table 1). PHYTOPLANKTON The microalgal community in Laguna de Rocha was represented by an assemblage of planktonic and benthic taxa, composed by a mixture of limnetic, brackish, and marine species. Bacillariophyceae was the richest group (53.7% among the 190 taxa

Phytoplankton of a Subtropical Coastal Lagoon

TABLE 2. Phytoplankton taxa that represented $10% of total biovolume (*) during the study period at stations South (S) and North (N). Taxa

Bacillariophyceae—Pennales Cylindrotheca closterium (Ehr) Reiman&Lewin Cylindrotheca gracilis (Bre´b) ex Ku¨tz Entomoneis alata var. alata (Ehr) Ehrenberg Entomoneis pulchra (Bail) Reim. Fragilaria sp. 1 Fragilaria sp. 2 Gyrosigma sp. 1 Navicula erifuga Lange-Bert. Navicula cf. symmetrica Patrick Navicula spp. Nitzschia circumsuta (Bailey) Grunow Nitzschia cf. frustulum (Ku¨tz) Grun Nitzschia levidensis Grunow Nitzschia palea/paleaceae Nitzschia reversa W. Sm. Nitzschia spp. Surirella brebissonii Krammer L-Bertalot Surirella splendida (Ehr) Ku¨tz Surirella sp. Synedra ulna (Nitsch) Ehr Tabularia affinis (Ag) Will&Round Tabularia fasciculata (Ag) Will&Round Bacillariophyceae—Centrales Aulacoseira granulata (Ehr) Simonsen Melosira dubia Ku¨tz Melosira moniliformis (Mu¨ller) Agardh Melosira moniliformis var. octogona (Grun) Husted Melosira sp. Paralia sulcata (Ehr) Cleve Skeletonema cf. costatum (Greville) Thalassiosira eccentrica (Ehr) Cleve Thalassiosira spp. Cryptophyceae Rhodomonas minuta Skuja Rhodomonas spp. Chroomonas cf. salina (Wislouch) Cryptomonas spp. Hillea sp. Dinophyceae Ceratium tripos (O Mu¨ller) Nitzsch Gymnodinium sp. 1 cf. Katodinium spp. Prorocentrum minimum (Pavillard) Schiller Peridiniales Euglenophyceae Eutreptiella cf. gymnastica Throndsen Eutreptiella sp. 1 Euglena acus Ehr. Euglena spp. Prasinophyceae Pyramimonas spp. Chlorophyceae Chlorogonium sp. 1 Volvocales (,10 mm) Small flagellates (,7 mm); diverse groups




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registered), followed by Cryptophyceae, small flagellates of diverse groups (MLD , 7 mm), Dinophyceae, Prasinophyceae, Euglenophyceae, Chlorophyceae, and Cyanobacteria (Table 2). Although


both stations shared a high number of taxa (50% of the total taxa identified), Chlorophyceae showed a higher number of freshwater taxa at station N (Scenedesmus spp., Closterium sp., Chlorella sp.), representing less than 1% of the total biovolume. The most frequent centric diatoms observed (e.g., Melosira spp., Pseudopodosira kosugii, and Paralia sulcata) were typical of shallow brackish systems. Among pennate diatoms, some benthic epipelic taxa were commonly registered (e.g., Fragilaria spp., Tabularia spp., Nitzschia spp., and Navicula spp.; Table 2). Within Dinophyceae, the euryhaline coastal Prorocentrum minimum was found mainly at the southern area during autumn and winter, associated with the marine intrusion. Average phytoplankton abundance for the whole study was similar at both stations and periods (K-W, p . 0.05; Table 3). Total biovolume varied from 0.05 to 27.83 mm3 l21 and did not show a defined seasonal pattern, when Bacillariophyceae was the dominant group (Fig. 4). No significant differences were detected between stations (K-W, p . 0.05), although when both periods were compared significant differences were found in total and relative biovolume of the main groups (Table 3, Fig. 4). The contribution of pennate diatoms was significantly higher during the first period at station S (K-W, H 5 8.514, p , 0.05; Table 3, Fig. 4). The second period was characterized by lower phytoplankton biovolume and significant higher contribution of Chlorophyceae (K-W, H 5 20.95, p , 0.0001) and Euglenophyceae (K-W, H 5 8.284, p , 0.05). Small flagellates of diverse groups were lower in the second period at both stations (K-W, H 5 24.395, p , 0.0001). Some of the main taxa within these flagellates were Eutreptiella cf., gymnastica, Eutreptiella sp., Chroomonas cf., baltica, Chroomonas spp., Hillea sp., Pyramimonas sp., and Chlorogonium sp. For the dominant species (.25% of total biovolume) there were a variation of two orders of magnitude in cell size (MLD: 8–248 mm) and S:V ratio (0.05–2.19 mm21). Specific biovolume ranged from 61 to 71 3 104 mm3 (average 5 3.5 3 104 mm3). Applying the classification of three life strategies, we determined that most of the species were C-, R-, CS-, or CR-strategists (e.g., Cyclotella atomus, Chaetoceros spp., Tabularia fasciculata, and Synedra ulna) (Figs. 5 and 6). C-strategists were more important in the marine influence area during the first period, decreasing their importance during the second period at both stations (Table 3). Few species corresponded to stress-tolerant S-strategists (S:V ratio ,0.3 mm21 and cell size .104 mm3), like Surirella splendida and Euglena cf., acusiformis, mostly found in the northern zone during period 1 (Figs. 5 and 6, Table 3).


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TABLE 3. Total phytoplankton abundance and biovolume (average (6SD)) and relative contribution of main taxonomic groups and life strategies (average) for stations South (S) and North (N) discriminated for periods 1 and 2. S1

Total Abundance (3 104 org l21) Total Biovolume (mm3 l21) Biovolume (%) Cyanobacteria Bacillariophyceae (Centrales) Bacillariophyceae (Pennales) Dinophyceae Cryptophyceae Prasinophyceae Chlorophyceae Euglenophyceae Flagellates Life strategies (%) C CR CS R S




226 (167) 189 (124) 359 (642) 330 (421) 1.9 (2.05) 1.1 (1.5) 2.8 (7.8) 1.2 (1.8) 0.9 33.0

0.1 39.2

0.5 25.7

0.8 16.6





28.5 3.0 0.2 3.1 3.6 8.3

2.8 22.1 0.2 12.1 11.8 3.2

8.9 16.2 0.9 1.0 7.4 9.0

16.9 15.0 0.3 8.5 13.6 2.1

42.6 13.9 28.3 15.2 0.0

11.5 48.6 30.4 7.8 1.7

7.0 9.9 53.8 9.2 20.1

11.0 24.3 41.6 12.6 10.4

The first four axes of the CCA analysis performed with species and environmental variables explained 64.8% of the total variance of the species matrix (Monte Carlo test was significant for the first and all axes, p , 0.01; Fig. 6, Table 4). The first axis, principally defined by the conductivity gradient, was constructed by K and DO and presented the strongest correlation between species and environmental variables (0.829) associated with the study at both stations. The second axis (correlation species environmental variables: 0.764) was defined by the nutrients RS and SRP and inversely by DIN (Table 4). Most samples from the first period were distributed toward the positive extreme of axis 1 in the CCA (Fig. 6), while the opposite occurred with the samples from the second period. The Cstrategists Melosira sp. and Hillea sp., the R-strategists S. ulna and T. fasciculata, the S-strategists Thalassiosira eccentrica, and some species with intermediate position like Thalassiosira sp.1 (CS), Melosira moniliformis (CS), Melosira dubia (CR), Prorocentrum minimum (CR), and Nitzschia spp. (CR) were associated with the period of higher conductivity and shallowness (Figs. 5 and 6). Surirella spp. (Sstrategist), and the fast growing and invasive T. fasciculata (R-strategist), Trachelomonas sp. (CS-strategist), Eutreptiella sp. 1, and Euglena spp. (CRstrategists), were associated with the second study period and higher pr and DIN and PRS concentrations. The CR-strategists Chroomonas spp. and Chaetoceros subtilis var. abnormis f. simplex, and dinoflagellates of the Order Peridiniales (CS-strate-

Fig. 4. Temporal variation of biovolume of main phytoplanktonic groups at South and North stations. Black bars: Pennate Bacillariophyceae, gray bars: Centric Bacillariophyceae, and white bars: other groups.

gists), were present under conditions of higher temperature and high RS concentration (second period). Some species of diverse life strategies were located near the center of the triplot (e.g., P. sulcata, M. moniliformis var. octogona, Cylindrotheca closterium, Euglena sp. 1, and Chroomonas sp. 1), indicating no association with the abiotic gradients, which is in good agreement with the presence of these taxa during the study in both stations (Figs. 5 and 6). Discussion Although poorly recognized, in many shallow systems resuspended meroplankton and epipelon may build up the pelagic community (Carrick et al. 1993; de Jonge and van Beukenson 1995; Schelske et al. 1995; Facca et al. 2002; Badylak and Phlips 2004). In our study, many cells identified in the phytoplankton community of Laguna de Rocha were mostly diatoms, typically epipelic and characterized by a small size. They appeared in the pelagic, favored by the shallowness of the lagoon, sediment type, wind intensity, and permanent mixing. Previous studies in this system showed the presence of epipelic species in the water column (e.g., Catenula adhaerens, Navicula recens, and Nitzschia frustulum; Conde et al. 1999). The high chlorophyll a values found on surface sediments (2.7–262 mg m22)

Phytoplankton of a Subtropical Coastal Lagoon

Fig. 5. Life strategies (C, S, and R) of phytoplankton from Laguna de Rocha as a function of morphology. Boxes indicate the range limit for MLD and S:V ratio for each strategy. Codes for species as follow: cyc: Cylindrotheca closterium, nit: Nitzschia palea/ paleaceae, nit1: Nitzschia cf., frustulum, sub: Surirella brebisonii, su: Surirella sp. 1, sus: Surirella splendida, syn: Synedra ulna, taf: Tabularia fasciculata, tab: Tabularia tabulata, cha: Chaetoceros sp. 1, chas: Chaetoceros subtilis var. abnormis f. simplex, memo: Melosira moniliformis var. octogona, med: Melosira dubia, mem: Melosira moniliformis, me: Melosira sp., pas: Paralia sulcata, thae: Thalassiosira eccentrica, tha: Thalassiosira, din2: dinoflagellate 2, prom: Prorocentrum minimum, pro: Protoperidinium, cry1, 2, 3, 4: Chroomonas sp. 1, 2, 3, 4, hill: Hillea sp., eug: Eutreptiella cf., gymnastica, eu: Eutreptiella sp., trac: Trachelomonas sp., and e1, 2, 3: Euglena sp. 1, 2, 3. (din2 and pro appear at the same place; nit behind eug).

suggested that benthos is an important source for the microalgal pelagic community (Conde et al. 1999). We consider that the identification of nontaxonomic groups, like the morphological-functional approach (Reynolds 1991), is an alternative to complement taxonomic analysis for depicting the phytoplankton community structure. This approach simplifies the universe of species in only three categories: C, S, and R, plus their intermediates (i.e., CR, CS). Although the CRS triangle model (proposed by Grime 1977) is general and has a low predictive value, it is still the best coherent theory for community ecology interpretations (Wilson and Lee 2000). We identified a wide range of different species, from limnetic to marine and from planktonic to epipelic, that fit in general to C, R, CR, and CS strategies, in agreement with Reynolds’ assumptions (Reynolds 1991, 1997; Smayda and Reynolds 2001). C-species are opportunistic invasive of high growth rates and they are expected to dominate in systems where a combination of high nutrient and


Fig. 6. Triplot diagram of two canonical correspondence analyses (CCA) for the first two axes. Codes for taxa as in Fig. 5 and for environmental variables as in Table 1. Samples from both stations as follow: black circles: South period 1; black triangles: South period 2; open circles: North period 1; and open triangles: North period 2.

light availability occurs (Reynolds 1997). As expected, S-strategists, favored under stable physical conditions and nutrient stress, in general were not prevalent in Laguna de Rocha. During the first period at station N, S-strategists reached 20% of the total biovolume (mostly represented by Surirella spp.). Our observation showed that the presence of these organisms covaried weakly with the expected nutrient depletion and stability of the water column assumed by the model. The particular phytoplankton composition of Laguna de Rocha is far from a typical planktonic community, for which this model has been developed. The scenario found for Laguna de Rocha resembles those of rivers, which are characterized by low retention times, turbidity, and mixed water column, where diatoms C- and R-strategists can be the dominant fraction (Reynolds et al. 1994). The same pattern was found in other shallow systems with continuous or daily mixing conditions like the eutrophic tropical Barra lagoon (Huszar et al. 1998) or the mesotrophic Monte Alegre Reservoir, where R-strategists dominated during mixing periods (Huszar et al. 1998). The relationship between the mixing and euphotic zones (Zmix:Zeu) in lakes has been pointed out as another driving factor of phytoplankton composition and abundance (Reynolds 1997). Fichez et al. (1992) showed that phytoplanktonic primary pro-


S. Bonilla et al.

TABLE 4. Results of canonical correspondence analyses (CCA) performed with biovolume of main phytoplankton taxa. Sum of all unconstrained eigenvalues: 5.128. The correlations of each variable with the first 3 axes are shown (statistical significance: 1.96), ns: not significant. Monte Carlo test was significant for the first (p , 0.005) and all (4) canonical eigenvalues (p , 0.005). Abbreviations as in Table 1. CCA main taxa 1

Eigenvalues Cumulative percentage of variance Species Species-environment relation Significant correlations of environmental variables K RS DO SRP pr Z T SS DIN pH








6.2 23.8

10.8 41.4

13.9 53.5

16.8 64.8

+0.64 ns 20.37 ns ns ns 20.13 ns 20.10 ns

ns +0.32 ns +0.39 ns ns ns ns 20.47 ns

ns +0.15 20.25 20.28 ns +0.56 ns ns ns ns

ns +0.06 20.19 20.36 +0.45 ns ns ns ns ns

duction and growth depend on the Zmix:Zeu ratio, and a ratio of 4 to 5 is the threshold value where net primary production becomes zero (Talling 1971). Although the limnetic station at Laguna de Rocha registered higher K d values than the brackish one because of fine sediment resuspension (Sommaruga and Conde 1990; Conde et al. 1999, 2000), in all cases more than 1% of incident PAR reached the bottom and Zmix:Zeu ratio was usually , 1. Consequently, PAR availability could be considered a minor factor controlling phytoplankton growth in this system. Temperature variation in Laguna de Rocha exhibited a similar pattern to other lagoons of the region (Seeliger et al. 1997). Due to the subtropical location of this system, temperature changes may be viewed as relatively modest in magnitude. As expected, no clear seasonal pattern was observed in the phytoplankton dynamics. Considering that temperature changes associated with seasonality are less relevant, Laguna de Rocha resembles a tropical system. Significant differences in total biovolume were detected in Laguna de Rocha between periods of different hydrology and connection with the ocean, suggesting that the frequency of exchange with the sea controls the phytoplankton biomass and prevents the development of microalgal blooms inside the lagoon. It has been pointed out that exchange with the ocean in coastal lagoons washes out organic matter, preventing eutrophication and

anoxia (Duarte et al. 2002; Suzuki et al. 2002). The development of blooms could be favored if isolation occurs for long periods. For example, the increment of nutrients and blooms of filamentous Cyanobacteria and diatoms at Imboassica lagoon (Brazil) were detected after 15 mo of isolation from the sea (Melo 2001). At the subtropical Indian River Lagoon (USA), flow-restricted areas can exhibit a residence time of up to 1 year, which promoted phytoplankton biomass accumulation (Badylak and Phlips 2004). In the CCA analysis, the first axis can be interpreted as the marine influence, while the relative contribution of RS, DIN, and SRP to the second axis indicates the biogeochemical component. These factors play a key role in phytoplankton composition and dominant groups (Reynolds 1997; Huszar and Caraco 1998). During the first period (high K and DIN; low pr, K d, and RS), brackish and marine Bacillariophyceae and P. minimum dominated the community. This CR-strategist dinoflagellate, potentially toxic (Steidinger 1983), is frequently abundant (5 3 106 org l21) during winter and spring along the Atlantic coast (Ferrari and Pe´rez 2002) and can be transported by marine intrusions inside the lagoon, where new environmental conditions can favor its growth. P. minimum is also present as a consequence of the marine intrusion in other coastal lagoons (Macedo et al. 2001; Melo 2001). During the second period (low K and DIN; high pr, K d, and RS), the relative contribution of flagellates (Cryptophyceae, Euglenophyceae, Prasinophyceae, and small flagellates) increased significantly. The concentration of DIN and SRP fluctuated widely along the study, probably due to water exchange, mineralization, and resuspension from the sediments (Pintos et al. 1991). Low DIN:SRP ratios (,5) during the second period suggested that nitrogen could be the principal limiting nutrient. Aubriot et al. (2004) suggested that limitation by phosphorus or nitrogen in Laguna de Rocha may be highly variable and closely related to the prevailing hydrological condition. The concentration of RS was always high at both stations and seemed to favor the dominance of diatoms. It has been recognized that the high availability of silica and high RS:DIN or RS:SRP ratios in coastal systems favor the dominance of diatoms and consequently prevent the development of nuisance algae like dinoflagellates and cyanobacteria (Officier and Ryther 1980; Conley and Malone 1992). Although Cyanobacteria was a minor group in our study, more recent data (2003 and 2004) indicate the occasional presence of Pseudanabaena cf., moniliformis and unicellular picocyanobacteria (Synechococcus sp. like) in high abundance (Hein and Piccini personal communication), suggesting recent changes in the input of nutrients

Phytoplankton of a Subtropical Coastal Lagoon

into the lagoon. In our study, phytoplankton biovolume (0.05–27.8 mm3 l21) was lower in comparison with other eutrophic coastal lagoons: Lagoa Imboassica (5.0–89.0 mm3 l21), a system with a similar connection pattern to the ocean as Laguna de Rocha (Melo 2001); Lagoa dos Patos (100– 1,500 mm3 l21), permanently connected with the ocean (Torgan 1997); Venice Lagoon (900– 3,000 mm3 l21), with residence times of up to few days (Facca et al. 2002); and Barra Lagoon (22.4– 38.3 mm3 l21), indirectly connected to the ocean (Huszar et al. 1998). Our results indicate that the phytoplankton community reflects firstly the hydrological state and secondly the nutrient status of the lagoon. Permanent mixing of the water column, sediment resuspension, low Zmix:Zeu ratios, and bidirectional horizontal flows are physical conditions selecting small unicellular planktonic and epipelic species, Cand R-strategists. High frequency of connection with the ocean limits high biomass accumulation. Nutrient dynamics and low conductivity explained the taxonomic composition and the general dominance of diatoms. The potential relevance of grazer control on the phytoplankton standing crop in Laguna de Rocha is presently unknown. It has been pointed out that the direct role of climate as a driving force for phytoplankton biomass and composition in coastal systems is a long-term perspective (Lehmann 2000). Local rainfall at Laguna de Rocha can affect the general behavior of the system and the phytoplankton dynamics in a long-term perspective. Under periods of low rainfall and higher marine influence, we expect Laguna de Rocha to present higher phytoplankton biovolume and to be dominated by pennate diatoms, euglenoids like Eutreptiella spp., and dinoflagellates such as P. minimum. Events of high rainfall and low conductivity would promote the dominance of flagellates, Cryptophyceae, freshwater Euglenophyceae, Prasinophyceae, and others typical of low salinity. Under this situation, total biovolume will reach lower values because of intense washout from the lagoon into the ocean. In good agreement, other studies showed that rainfall can influence salinity and nutrient status that will, in turn, affect the phytoplankton community (Badylak and Phlips 2004). Dinoflagellate blooms occurred during a year of high rainfall (El Nin ˜ o event 1997–1998) in a flowrestricted area of the subtropical Indian River Lagoon (USA), which were substituted by picocyanobacteria blooms in the following year with lower rainfall (Badylak and Phlips 2004). The rainfall pattern on the southeastern coast of South America is tightly coupled to El Nin ˜ o-Southern Oscillation dynamics (Abreu and Castello 1997). This may be relevant for Laguna de Rocha in a long-term


perspective, according to the expected decrease of river flows in eastern South America for the next decades (Genta et al. 1998), which can affect the opening dynamics of choked coastal lagoons and their overall productivity. ACKNOWLEDGMENTS We thank Valeria Hein for field and laboratory assistance, Nora Maidana for diatom identification, and Clarisse Odebrecht and Vera Huszar for comments and suggestions that improved the quality of the manuscript. This study was supported by grants from DINACYT-Uruguay (1099, 2086), PEDECIBA, CSIC-UDELAR (C-09), and Red Latinoamericana de Bota´nica (Binac 99-1).

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SOURCES OF UNPUBLISHED MATERIALS RODRI´GUEZ-GALLEGO, L. personal communication. Seccio´n Limnologı´a, Facultad de Ciencias, Igua´ 4225, 11400-Montevideo, Uruguay. HEIN, V. personal communication. Seccio´n Limnologı´a, Facultad de Ciencias, Igua´ 4225, 11400-Montevideo, Uruguay. PICCINI, C. personal communication. Instituto de Investigaciones Biolo´gicas Clemente Estable, Avda. Italia 3318 Montevideo11600, Uruguay. Received, February 22, 2005 Revised, July 6, 2005 Accepted, August 10, 2005

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