Phytoplankton seasonal variation in a shallow stratified ... - UCB

Hydrobiologia (2008) 600:267–282 DOI 10.1007/s10750-007-9240-9

PRIMARY RESEARCH PAPER

Phytoplankton seasonal variation in a shallow stratified eutrophic reservoir (Garças Pond, Brazil) Ba´rbara M. Fonseca Æ Carlos E. de M. Bicudo

Received: 10 July 2007 / Revised: 1 November 2007 / Accepted: 12 November 2007 / Published online: 5 December 2007 Ó Springer Science+Business Media B.V. 2007

Abstract This study aimed at describing the phytoplankton dynamics and structure in a shallow eutrophic reservoir, the Garças Pond, located in the Parque Estadual das Fontes do Ipiranga (23°380 40.600 S, 46°370 28.000 W), in the Municipality of Saõ Paulo, southeast Brazil. Samples were collected monthly from January to December 1997 in five depths (subsurface, 1 m, 2 m, 3 m, and 20 cm above the bottom) in the pelagic zone (Zmax = 4.7 m). Abiotic variables studied were: water temperature, turbidity, transparency, conductivity, pH, dissolved oxygen, alkalinity, inorganic carbon, and N and P dissolved and total forms. Altogether 236 phytoplankton taxa distributed among 10 classes were identified. Phytoplankton seasonal and vertical variation was related to shifts in the water chemical features as a consequence of a warm-wet season with stratified water column (phase 1, January–March and September– December) alternating with a cool-dry season with mixed water column (phase 2, April–August). There

Handling editor: J. Padisak B. M. Fonseca (&) Curso de Cieˆncias Biolo´gicas, Universidade Cato´lica ´ guas Claras, Brasilia, DF de Brası´lia, QS 07, Lote 1, A 71966-700, Brazil e-mail: [email protected] C. E. de M. Bicudo Instituto de Botaˆnica, Seçaõ de Ecologia, Caixa postal 3005, Sao Paulo, SP 01061-970, Brazil

were shifts in cyanobacterial dominance over the entire year. During phase 1, Raphidiopsis/Cylindrospermopsis was one of the most important taxon. During phase 2, Raphidiopsis/Cylindrospermopsis biomass decreased, whereas richness and diversity increased and diatoms were relatively abundant. In September, when the water column was markedly stratified, a cyanobacterial bloom (Sphaerocavum brasiliense) occurred. Changes in water chemical variables caused by the bloom allowed recognition of a phase 3, in which pH and chlorophyll a, TP and CO2concentration reached their highest values. 3 According to Reynolds and collaborators’ functional groups approach, phase 1 was marked by groups S/ W1/W2/H1/Y, phase 2 by groups K/LM/LO/D/P/X1/ F, and phase 3 by group M. This sequence was corroborated by canonical correspondence analysis (CCA) results. Keywords Community structure and dynamics Functional groups Sphaerocavum brasiliense Raphidiopsis mediterranea Cylindrospermopsis raciborskii

Introduction During the last two decades, shallow lakes metabolism was frequently addressed (Scheffer, 1998; Scheffer & van Nes, 2007). Their responses to eutrophication can be catastrophic, mainly due to

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268

the intense water–sediment interaction (Bicudo et al., 2007). Padisa´k & Reynolds (2003) discussed the role of the ecosystem depth in its functioning and introduced the concept of functional shallowness applied to discontinuously mixed water bodies. According to the latter authors, however, some systems shallower than 10 m can stratify and behave like deep lakes. Therefore, shallowness is not a function only of the system’s absolute depth value, since factors such as basin morphology and shelter degree also have to be considered. Some functional shallow lakes do not fit into the classical relationship models among biomass, phytoplankton composition, and nutrient supply (Jensen et al., 1994). Phytoplankton community structure responds to trophic and seasonal gradient through changes in species composition and quantitative ecological traits as biomass, species richness, and diversity (Watson et al., 1997). Quantification of these ecological processes is essential for the establishment of predictive models applied to natural communities (Reynolds, 2006). An increasing number of authors have emphasized species’ morphofunctional attributes as important tools in phytoplankton dynamics studies (Huszar & Caraco, 1998; Reynolds et al., 2002; Salmaso & Padisa´k, 2007). Many studies described temporal phytoplankton patterns in lakes with varying mixing regimes. These include functional shallow lakes such as Balaton (Zmax = 11 m; Padisa´k, 1992) and Rodo´ (Zmax = 2.5 m; Kruk et al., 2002), as well as functional deep lakes as Garda (Zmax = 350 m; Salmaso, 2003) and Maggiore (Zmax = 370 m; Morabito et al., 2003). Notwithstanding, this matter is far from being exhausted. Accelerated rates of anthropogenic eutrophication are continuously demanding management strategies applied to eutrophic reservoirs, with particular emphasis to those in tropical countries. In Brazil, phytoplankton communities from eutrophic urban reservoirs such as Guarapiranga (Beyruth, 2000), Billings (Carvalho et al., 1997), Pampulha (Figueredo & Giani, 2001), and Paranoa´ (Branco & Senna, 1996) are among the most studied ones. Recently, hypereutrophic lakes from the northeastern region of the country, as the Tapacura´ (Bouvy et al., 2003) and the Gargalheiras (Chellapa & Costa, 2003) have also been explored, mainly after Caruaru’s

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Hydrobiologia (2008) 600:267–282

incident, when people died as a consequence of liver failure caused by microcystin toxin from cyanobacterial blooms (Koma´rek et al., 2001). Garças Pond phytoplankton was already described from various aspects like taxonomy (Azevedo & Sant’Anna, 1999, 2003; Koma´rek & Azevedo, 2000; Tucci et al., 2006), ecology (Sant’Anna et al., 1989, 1997; Ramı´rez & Bicudo, 2002; Tucci, 2002; Tucci & Sant’Anna, 2003; Fonseca, 2005; Ramı´rez & Bicudo, 2005; Crossetti & Bicudo, 2005a, b; Crossetti, 2006) and toxicology (Sant’Anna & Azevedo, 2000). The reservoir’s limnological features changed substantially over the last 10 years, especially due to the undesirable side effects of the water hyacinth control. Bicudo et al. (2007) described the mechanisms underlying limnological variations in the reservior during the period 1997–2004. Present article aims at describing the phytoplankton seasonal and vertical variation in the Garças Pond, with emphasis on its dynamics and structure before the water hyacinth proliferation and in relation to the abiotic environment.

Study area Garças Pond (23°380 40.600 S, 46°370 28.000 W) is located in the Parque Estadual das Fontes do Ipiranga Biological Reserve (PEFI; 526 ha; 798 m.a.s.l) situated in the Municipality of Saõ Paulo, southeastern Brazil. See Bicudo et al. (2007) and Crossetti & Bicudo (2005a) for site location. The mean annual precipitation is 1,368 mm, the mean air temperature of the coldest month (July) is 15°C, and the mean temperature of the warmest months (January–February) is 21.4–21.6°C (Santos & Funari, 2002). Climate of the area is tropical (Conti & Furlan, 2003) and wind speed is commonly low (\2.5 m s-1). Although locally called Garças Pond, the water body is, in fact, a reservoir recently classified as eutrophic/hypereutrophic (Bicudo et al., 2006). It has a surface area of 88,156 m2, a volume of 188,785 m3, a mean depth of 2.1 m, a maximum depth of 4.7 m, a mean theoretical residence time of 71 days (Bicudo et al., 2002) and is polymictic according to Lewis’ classification (Bicudo et al., 2002). Garças Pond has one outlet and seven tributaries, four of which carring sewage (Henry et al., 2004).


Material and methods Samplings were performed monthly from January to December 1997 at five depths at the deepest site of reservoir. Water samples were gathered with a van Dorn sampler. Temperature, pH, and conductivity were measured in the field using standard electrodes (Yellow Spring Instruments). Water relative thermal resistance (RTR) was calculated for every 50 cm depth (Dadon, 1995). The mixing zone (Zmix) was identified through temperature profiles considering density gradients [0.02 kg m-3 m-1 (Reynolds, 1984). Euphotic zone (Zeu) was calculated as 2.7 times the Secchi depth (Cole, 1983). The following variables were measured on the sampling day: alkalinity (Gol2terman & Clymo, 1971), free CO2, HCO3 and CO3 (Mackereth et al., 1978), DO (Golterman et al., 1978), NH+4 (Solorzano, 1969), NO2 and NO3 (Mackereth et al., 1978), and soluble reactive phosphorus (SRP) (Strickland & Parsons, 1965). Unfiltered samples were used for total nitrogen (TN) and total phosphorus (TP) determinations (Valderrama, 1981) within at most 30 days from collecting date. NH+4 –N concentrations were added to obtain final TN levels. Chlorophyll a analyses corrected for phaeophytin were carried out at most within 1 week from the sampling day using 90% ethanol extraction (Sartory & Grobbelaar, 1984). Phytoplankton quantitative investigation was carried out according to Utermo¨hl (1958). Sedimentation time followed Lund et al. (1958). The number of settling units counted in each individual sample varied according to species accumulation curve. The same chamber volume (2 ml) was used throughout the year and at least 40 fields were counted for each chamber (Rott, 1981). Biovolume was obtained by geometric approximation, multiplying each species’ density by the mean volume of its cells considering, whenever possible, the mean dimension of 30 individual specimens of each species (Sun & Liu, 2003). Phytoplankton functional groups were defined according to Reynolds et al. (2002) from the species that contributed with at least 5% of the relative biovolume in at least one sample. Such species were considered P as dominant. Shannon-Wiener Index (H 0 ¼ ½pi log2 pi ) was used to estimate diversity (Shannon & Weaver, 1949). Spearman Rank Correlation was used to test association between abiotic and biotic variables.

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Multivariate descriptive analysis was carried out by applying principal component analysis (PCA) to the abiotic data using a covariance matrix with data transformed by ranging. Sample units ordination using canonical correspondence analysis (CCA) was perfomed for five abiotic variable, i.e., the ones with the greatest correlation with the first 2 axes of PCA, thus avoiding redundant variables, and 13 phytoplankton functional groups. Samples (n = 36) were selected from the euphotic zone (subsurface, 1 and 2 m). For CCA analysis, pffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi biological data were transformed by ½ x þ 0:5 and abiotic data were transformed by ranging. Monte Carlo test of significance based on 999 permutations tested the hypothesis (Ho) of no relationship between the functional groups and the environmental data. Software used for the transformed data was FITOPAC (Shepherd, 1996) and PC-ORD version 4.0 for Windows (McCune & Mefford, 1997) for multivariate analyses. Results were considered significant when P \ 0.05.

Results Abiotic variables Variation of water temperature and dissolved oxygen profile over the year allowed definition of two distinct periods based on the reservoir mixing conditions: (1) from January to March and from September to December (phase 1), when the reservoir was often stratified, and (2) from April to August, when the reservoir was often mixed (phase 2) (Fig. 1). During phase 1, RTR reached its greatest values and Zmix the smallest ones (\2 m). Thermal stratification was followed by chemical stratification, mainly for TN, SRP, NH+4 , conductivity, and DIC (Fig. 2). These variables reached their greatest values in the bottom samples from January to March and from September to December (Table 1). Close to bottom, oxygen was completely exhausted in association with the highest values of DIC, NH+4 and conductivity suggesting intensive decomposition at the bottom of reservoir during phase 1. During phase 2, Zmix usually reached the bottom of reservoir and all variables above were homogeneously distributed in the water column (Fig. 2). Zeu never reached the bottom of reservoir

123

270 O2 (mg.L-1) 0

2

4

6

O2 (mg.L-1) 8

10

0

2

16

18

20

22

4

24

16

18

20

22

24

16

2

Depth (m)

1

Depth (m)

1

2

3

Jan 10

20

30

Feb

4 0

40

2

4

10

18

6

20

0

10

22

2

16

20

30

40

0

4

6

10

18

20

22

24

Depth (m)

Depth (m)

Apr 20

2

30

May

4

40

0

10

O2 (mg.L-1)

18

20

10

22

0

2

16

20

30

0

40

4

6

10

18

20

22

24

Depth (m)

Depth (m)

Jul

2

20

30

Aug

4

40

0

10

O2 (mg.L-1) 10

0

2

Temperature ( ° C) 16

18

20

22

16

20

30

0

40

4

6

10

18

20

22

24

16

Depth (m)

Depth (m)

2

3

Oct 30

40

Temperature

24

20

30

40

2

4

6

8

10

18

20

22

24

2

3

Nov

4

RTR

22

Temperature ( ° C)

1

20

10

0

1

10

20

O2 (mg.L-1) 8

1

3

10

RTR

0

2

8

Sep

0

0

6

4


40

2

0

4

18

O2 (mg.L-1) 8

30

4

RTR

6

24

3

RTR

4

20

2

16

3

4

22

Temperature ( ° C)

1

2

10

0

1

0

20

O2 (mg.L-1) 8

1

3

10

RTR

0

2

8

Jun

0

10

6

4

Temperature ( °C) 24

40

2

0

0

18

O2 (mg.L-1) 8


4

RTR

6

30

3

RTR

4

2

16

3

2

20

Temperature ( ° C)

1

0

10

0

1

4

24

O2 (mg.L-1) 8

1

3

22

RTR

0

2

10

Mar

Temperature ( °C) 24

8

4

0

10

20

O2 (mg.L-1) 8

6

2

0

0

18

RTR


4

3

O2 (mg.L-1) 0

2

Temperature ( ° C)

1

RTR

Depth (m)

0

0

0

Depth (m)

10

0

4

Depth (m)

O2 (mg.L-1) 8

0

3

123

6

Temperature ( °C)

Temperature ( °C)

Depth (m)

Fig. 1 Vertical profiles of water temperature (°C), dissolved oxygen (mg l-1) and water relative thermal resistance (RTR). Mixing zone is identified by an arrow


0

10

20

30

40

50

Dec

4 60

0

RTR

Dissolved oxygen

10

20

30

RTR

RTR

Zmix

40

Phase 1

Phase 3

Phase 2

Phase 1

242 222 202 182 162 142 122 102 82 62

2 3 B

1 2 3 B

(c) S Depth (m)

1 2 3 B

(d) S Depth (m)

1 2 3 B

Depth (m)

(e)

S 1 2 3 B

Depth (m)

(f)

S 1 2 3 B Jan

Feb Mar Apr May Jun

Jul

40 36 32 28 24 20 16 12 8 4

SRP (u g L- 1)

13150 12150 11150 10150 9150 8150 7150 6150 5150 4150 3150 2150 1150 150

11000 9800 8600 7400 6200 5000 3800 2600 1400 200

Ammonium (ug L -1)

Depth (m)

(b) S

129 119 109 99 89 79 69 59 49 39 29

T ot al CO2 ( mg L -1)

Depth (m)

1

488 428 368 308 248 188 128 68 8

Nitrate (ug.L-1)

(a) S

271 Total nitrogen (ug L-1) To ta l p ho sp h orus (u g L- 1 )


Aug Sep Oct Nov Dec

Month

Fig. 2 Depth-time diagram of (a) total phosphorus (lg l-1), (b) total nitrogen (lg l-1), (c) soluble reactive phosphorus (lg l-1), (d) ammonium (lg l-1), (e) total CO2 (mg l-1) and (f) nitrate (lg l-1) in the Garças Pond during 1997. Temporal phases are indicated by vertical lines

during the study (maximum value = 2.5 m, in June); Zeu:Zmix ratio was, in general, B1. The highest values of DO were measured in September at the surface (10.6 mg l-1). At the end of

Table 1 Mean values of water variables in Garças Pond, during phases 1 (n = 30), 2 (n = 25), and 3 (n = 5) Variable

Phase 1

Phase 2

Phase 3

Water temperature (°C)

22.4

18.6

18.3

pH

6.9

6.9

7.8

Conductivity (lS cm-1)

150.9

140.0

146.6

Turbidity (NTU)

18.9

13.6

27.3

Dissolved oxygen (mg l-1)

3.6

4.9

5.5

Alkalinity (mEq l-1)

0.9

0.6

0.8

-1

Total CO2 (mg l )

57.9

36.8

37.4

Free CO2 (mg l-1)

16.1

9.0

4.4

-1 HCO3 (mg l )

57.9

38.5

45.2

-1 CO23 (mg l )

0.022

0.013

0.455

N–NH+4 (lg l-1)

2,957.6

1,209.3

2,052.3

N–NO2 N–NO3

(lg l )

22.2

27.9

\5.0

(lg l-1)

125.0

342.1

\8.0

DIN (lg l-1)

1,938.7

911.0

1,834.9

TN (lg l-1) SRP (lg l-1)

1,166.2 7.1

668.3 \4.0

226.6 7.1

-1

TDP (lg l-1)

19.6

12.3

17.5

TP (lg l-1)

115.9

95.0

178.8

TN:TP molar ratio

66.6

28.9

30.9

DIN:SRP molar ratio

780.3

637.3

440.9

SiO2 (mg l-1)

2.1

1.7

1.2

Chlorophyll a (lg l-1)

48.9

46.3

94.3

Biovolume (mm l )

18.3

20.6

67.4

Density (ind ml-1)

12,173

9,763

5,720

3 -1

winter and beginning of spring, cyanobacteria bloomed in the reservoir. Water chemical features were strongly affected by the high algal biomass and a third phase was recognized in the Garças Pond during September. During the algal bloom, TP (269 lg l-1) and pH (8.8) reached their highest values and NO2 and NO3 concentrations fall close to zero. Phase 3 coincided with phase 1 in regard to thermal profile. TN:TP molar ratio in the euphotic zone (subsurface, 1 and 2 m) was always below 60, with maxima from March to May and in October (Fig. 3). High DIN:SRP molar ratio was recorded during phase 2, although it peaked in October (Fig. 3). PCA using 14 abiotic variables and chlorophyll a explained 59% of data variability in the first 2 ordination axes (Fig. 4). The following variables were the most important ones (r [ 0.7) for axis 1 ordination: TN, NH+4 , free CO2, conductivity, DO,

123

D IN :S R P m o la r ra tio

T N :T P molar ra tio

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Hydrobiologia (2008) 600:267–282 60 54 48 42 36 30 24 18 12 6 0

2000 1800 1600 1400 1200 1000 800 600 400 200 0

Phase 1

Phase 2

mixing and stratification patterns explained axis 1 ordination. Samples from euphotic zone, mainly from phase 2 were, in general, placed on the negative side of axis 1 associated to higher DO values, while most of the bottom samples (except April, June, and August) were placed at the positive side of this axis and they were associated to high TN, NH+4 , free CO2, and conductivity values. Axis 2, on the other hand, ordinated samples by phases: phase 2 samples were placed at the positive side of the axis associated to high NO3 and NOvalues. Phase 3 samples were associated to high 2 TP and pH values on the opposing side and phase 1 samples grouped at the central part of the graph.

Phase 1

Phase 3

(a)

(b)

Jan

Feb

Mar

Apr

May

Jun

Jul

Aug

Sep

Oct

Nov

Dec

Month Subsurface

1m

Biotic variables

2m

Fig. 3 Seasonal variation of nutrients molar ratios considering (a) total and (b) dissolved forms (NT:TP and DIN:SRP) in the euphotic zone of Garças Pond. Temporal phases are indicated by vertical lines

Altogether 236 phytoplankton taxa including species and varieties were identified, which were grouped in 10 taxonomical classes. Chlorophyceae was the most representative class (97 taxa), followed by Cyanobacteria and Euglenophyceae (29 taxa each). The most frequent taxa were: Chlorella vulgaris, Trachelomonas volvocinopsis, Merismopedia glauca,

and SRP. For axis 2, however, NO2 , NO3 , and TP were the variables that contributed most (r [ 0.7) (Fig. 4). Vertical variation originated by seasonal

Fig. 4 Biplot of PCA for abiotic variables. Two letters in sample unit plots represent month (ja = January, fe = February, etc.)

NO3 jn jn jn jn jn jl jl

jl

Phase 2

NO2

jl

0,5

jl

Axis 1 (36%) -1,0

ma ma ma ma au auau ap au ap au ap ap ap

mr ma mr

pH

se

fe

mr

de se 0,0 oc fe de fe oc oc no oc ja de no no ja ja

DO

mr

fe

oc no ja

se

fe

CO2 TN Si cond SRP 1,0 NH4 de PDT

mr

no

2,0

de

-0,5

chlo-a

turb

TP

Axis 2 (23%)

se se

Depths Subsurface 1m 2m 3m Bottom

Phase 3

-1,5

Surface

123

Phase 1

ja

Bottom

Hydrobiologia (2008) 600:267–282 100%

Subsurface

80% 60% 40% 20% 0% 100% Bottom

80% 60% 40% 20% 0% Jan Feb Mar Apr May Jun Jul Ago Sep Oct Nov Dec Cyanophyceae Euglenophyceae Others

Dinophyceae Chlorophyceae

Cryptophyceae Bacillariophyceae

Phase 2

Phase 1

Phase 3 Phase 1

(b) S

144

12 11 10 9 8 7 6 5 4 3 2 1 0

Depth (m)

B

144 136 128 120 112 104 96 88 80 72 64 56 48 40 32 24 16 8 0

S. brasiliense (mm3 L-1)

S

Raph/Cylin (mm3 L -1)

(a)

Total biovolume (mm3 L-1)

Fig. 5 Seasonal and vertical variation of phytoplankton taxonomic classes relative contribution to total biovolume in the Garças Pond during 1997. To save space, just subsurface and bottom data are shown

1

2 3

136 128 120 112 104 96 88 80 72 64 56 48 40 32 24 16 8 0

Depth (m)

1

2 3

B

(c)

S

1

Depth (m)

Microcystis aeruginosa, Sphaerocavum brasiliense, Monoraphidium contortum, Cryptomonas erosa, and Aphanocapsa elachista, which were present in more than 90% of samples. Chlorophyll a mean annual value (n = 60) was 51.6 lg l-1 and it maximized in September during the cyanobacterial bloom at 218.3 lg l-1. Density and biovolume annual mean values (n = 60) were, respectively, 10,683 ind ml-1 and 23 mm3 l-1. Greatest density values were measured in January (45,269 ind ml-1) (phase 1), whereas the greatest biovolume one (148 mm3 l-1) was registered during the cyanobacterial bloom, in September (phase 3). The maximum values of chlorophyll a, density, and biovolume were all measured at the subsurface. In general, higher values of these variables were observed between subsurface and 2 m depth, mainly during phases 1 and 3, when the water column was thermally and chemically stratified. Species richness was high during phases 1 and 2, with a mean of 55. During phase 1, richness vertical profile followed the thermal one, decreasing sharply from subsurface to the bottom of reservoir. During phase 2, however, stratification being absent, richness values were homogeneous throughout the entire water column, although the euphotic zone did not reach the 3 m. The highest diversity was found in phase 2 with a maximum of 3.83 bits mm-3, in June, 2 m. Phase 3 showed the lowest diversity values, especially in the September subsurface sample (0.36 bits mm-3). Cyanobacteria contributed most to phytoplankton biovolume due to their bloom in September. They were positively correlated with pH (rs = 0.6), temperature (rs = 0.5), DO (rs = 0.6) and TP (rs = 0.7), and negatively with NO3 (rs = -0.6), NO2 (rs = -0.6), + TN (rs = -0.4), NH4 (rs = -0.4), NT:TP ratio (rs = -0.6) and free CO2 (rs = -0.5). Cyanobacteria were followed by Dinophyceae, Chlorophyceae, Euglenophyceae, Cryptophyceae, and Bacillariophyceae in dominance rank and relative contribution of all classes mentioned above was [90% in all samples (Fig. 5). Thirteen functional groups were found: M, S, H1, K, LM, LO, Y, W1, W2, D, P, F, and X1 (Table 2). Group M represented by Sphaerocavum brasiliense (Fig 6), Microcystis aeruginosa, and Microcystis panniformis was the most important one. During phase 1, biovolume relative contribution of group M

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2 3

B Jan

Feb

Mar

Apr

May

Jun

Jul

Aug

Sep

Oct

Nov

Dec

Month

Fig. 6 Depth-time diagram of (a) total biovolume (mm3 l-1), (b) Sphaerocavum brasiliense (mm3 l-1) and (c) Raphidiopsis/ Cylidrospermopsis (mm3 l-1)

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Table 2 Selected species from Garças Lake phytoplankton community based on biovolume [5% in at least one unit sample and its functional group relative contribution during phases 1, 2, and 3 Species

Microcystis aeruginosa (Ku¨tzing) Ku¨tzing M. panniformis Koma´rek et al.

Group

(%) 1

2

3

M

43.6

50.2

93.0

S

16.1

7.5

0.2

Sphaerocavum brasiliense Azevedo & Sant’Anna Raphidiopsis/Cylindrospermopsis Geitlerinema unigranulatum (Singh) Koma´rek & Azevedo Planktothrix agardhii (Gomont) Koma´rek & Anagnostidis Anabaena planctonica Brunnthaler

H1

0.6

0.1

0.0

Aphanocapsa elachista West & West A. incerta (Lemmermann) Cronberg & Koma´rek

K

0.7

6.3

1.2

Lo

1.6

0.3

0.5

LM

7.5

13.0

0.4

Ulnaria acus (Ku¨tzing) M. Aboal Fragilaria rumpens (Ku¨tzing) G. W. F. Carlson

D

0.5

2.9

0.0

Botryococcus braunii Ku¨tzing

F

0.8

0.3

0.4

Closteriopsis acicularis (G. M. Smith) Belch & Swale Closterium gracile Bre´bisson ex Ralfs

P

4.0

0.4

0.3

Euglena acus Ehrenberg

W1

3.4

0.2

0.0

W2

7.0

2.6

0.8

Y

8.7

6.5

0.5

X1

0.8

0.2

0.0

Cyanodictyon sp. 1 Merismopedia glauca (Ehrengerg) Ku¨tzing M. tenuissima Lemmermann Gymnodinium sp. 1 Peridinium cinctum (Mu¨ller) Ehrenberg Peridinium willei Huitfeld-Kaas

E. proxima Dangeard E. splendens Dangeard Trachelomonas hispida (Perty) Stein emend. Deflandre T. kellogii Skvortzov emend. Deflandre T. volvocinopsis Swirenko Cryptomonas curvata Ehrenberg emend. Penard C. erosa Ehrenberg C. marssonii Skuja Ankistrodesmus gracilis Corda sensu Korsˇikov Chlorella vulgaris Beijerinck Chlorococcum infusionum (Schrank) Meneghini Crucigenia tetrapedia (Kirchner) West & West Micractinium pusillum Fresenius Monoraphidium contortum (Thuret in Brbisson) Pseudodidymocystis fina ((Koma´rek) Hegewald & Deason) Scenedesmus ecornis (Ehrenberg) Chodat

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was around 40%. From phase 2 up to phase 3, contribution of codon M gradually increased exceeding 90% of the total biovolume during September (Table 2). The M group was positively correlated to pH (rs = 0.5), DO (rs = 0.6) and TP (rs = 0.6), and negatively to temperature (rs = -0.5), NO2 (rs = -0.6), NT:TP ratio (rs = -0.6), and free CO2 (rs = -0.4). The S functional group represented by Raphidiopsis/ Cylindrospermopsis (Fig 6), Planktothrix agardhii, and Geitlerinema unigranulatum was also important to Garças Pond phytoplankton community. The expression Raphidiopsis/Cylindrospermopsis is used to stress extreme difficulties in distinguishing Raphidiopsis mediterranea and Cylindrospermopsis raciborskii (see Section ‘‘Discussion’’ later). Their highest contribution was found during phase 1, when it reached 16.1% of the total biovolume. In September (phase 3), however, S group was virtually absent, contributing with 0% for total biovolume. The S group positively correlated with temperature (rs = 0.7) and SRP (rs = 0.7), and negatively with DIN (rs = -0.38). Cyanobacteria belonging to groups H1 (Anabaena planktonica), K (Aphanocapsa incerta), and LO (Merismopedia glauca) were also recorded but with smaller biomasses than members of S and M groups. They contributed with [5% for total biovolume in only 16% of all samples. K group contribution was particularly high during phase 2, when it represented 38% of July bottom layer total biovolume. Latter group showed significant positive correlation with Zmix (rs = 0.8) and NO3 (rs = 0.6), and significant negative correlation with temperature (rs = -0.8) and SRP (rs = -0.5). LM group was present all the year, as well as Y group. W1 and W2 groups’ contribution were especially high in March, when they reached together 47% of total biovolume at 3 m depth. Although diatoms from D group contributed little to the total biovolume (\1% in 80% of all unit samples), they had a pronounced seasonality, with highest values during phase 2, reaching 18.5% in July 2 m.

Integrated analysis of abiotic and phytoplankton functional groups CCA eigenvalues for axes 1 and 2 were 0.070 and 0.013, respectively, explaining 50% of total

275

variance on the first 2 axes. The hypothesis of no relationship between the functional groups and the environmental data was rejected (P \ 0.05, according to Monte Carlo test). Pearson environment-species correlation for the two significant axes was high ([0.7) (0.864 and 0.754, respectively), indicating a strong correlation between abiotic variables and the phytoplankton functional group patterns. Temperature and pH were the most important variables to axis 1 ordination according to canonical coefficients and intra-set correlations (Table 3; Fig. 7). Their vectors were located at opposite sides of the graph, associated with a gradient from phase 1 (left side) to phase 3 (right side). Sample units from phase 2 were concentrated in the center of the graph. Functional groups showing highest correlation with axis 1 were M (r = 0.85), which occurred under high pH values during phase 3, and S (r = -0.51), associated to higher temperature during phase 1. Axis 2 represented differences in mixing conditions. Free CO2 was the most important variable (canonical coefficients and intra-set correlations), followed by pH and DIN. In general, sample units from stratified months (phases 1 and 3) were on the positive side of axis 2, while sample units from mixing months (phase 2) were on the negative side, associated with high free CO2 and DIN concentrations. Functional groups S (r = 0.48) and K (r = -0.47) exhibited the highest correlations with axis 2.

Table 3 CCA synthesis for data from 5 abiotic variables and 13 functional groups in euphotic zone (n = 36) Axis 1 Canonical coeficient

Correlation coefficient (intra-set)

Axis 2

pH

0.660

0.469

TP

0.582

0.161

Free CO2

-0.392

-0.527

Temperature

-0.592

0.420

DIN

-0.029

-0.433

pH

0.764

0.622

TP

0.673

0.213

Free CO2

-0.453

-0.699

Temperature

-0.686

0.557

DIN

-0.034

-0.574

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Fig. 7 Biplot of CCA for five abiotic variables (temp = temperature, TP = total phosphorus, DIN = dissolved inorganic nitrogen, free CO2 and pH) and 13 phytoplankton functional groups (j) from the euphotic zone (subsurface, 1 and 2 m) in the Garças Pond during 1997 (n = 36)

2,0

Axis 2

276

Stratification

1,0

pH

temp S H1 W2 W1 Y 0,0 F D Lm 0K Lo X1 P

-2

TP Axis 1

M 2

DIN free CO2

Phases 1 2 3

-1,0

Mixing

-2,0

Phase 1

Discussion Similarly to temperate lakes, tropical ones also may experience seasonal climatic variations that determine physical and chemical changes. Such variations, however, differ in amplitude and intensity (Talling, 1969). Only equatorial lakes seem dominated by daily variations (Ganf, 1974). Two climatic periods could be defined from the present study, i.e., a warm-wet period from October to March and a cool-dry one from April to August. September was a transition month with high temperature and dry weather. This pattern is described for many aquatic environments in the Southern Hemisphere (Ashton, 1985). The lowest air temperatures during coldest months led to an increase of water density allowing complete mixing of Garças Pond. During the warm-wet spring/summer period, however, high water temperatures resulted in relatively stable water column stratification. Despite the shallowness of the Garças Pond, it was persistently stratified for a few weeks during the spring and summer like a typical discontinuous polymictic reservoir (Ramı´rez & Bicudo, 2002). A

123

Phase 2

Phase 3

similar stratification pattern was observed in other shallow reservoirs located in the same geographic region (Lopes et al., 2005; Bicudo et al., 2002). In this study, annual fluctuation in mixing patterns was a key factor triggering phytoplankton seasonal variation. Similar results have been reported for Ninfeías Pond, which is shallower than 5 m and located in \1 km distance from Garças one (Fonseca, 2005). According to Padisa´k & Reynolds (2003), the essential property of a shallow lake is that most, if not all, of the bottom sediment surface is frequently contiguous with the open-water. In this regard, Garças Pond can be considered as functionally deep during phases 1 and 3, when thermal stratification was stable enough to segregate bottom water layers with intensive decomposition. It is, however, likely that small amounts of nutrients were released to the surface from the bottom through atelomixis, a very common phenomenon in the tropics (Lopes et al., 2005). Chemical and biological features related to complete mixing occurred in the Garças Pond only during phase 2. Cyanobacteria dominated the Garças Pond phytoplankton community with [50% of total biomass

Hydrobiologia (2008) 600:267–282 Fig. 8 Synthesis diagram showing main abiotic and biological changes during the year 1997 in the Garças Pond

277

↓ Temperature Mixing ⇓

↑ Temperature Stratification ⇓

↓ nutrients ↑ dissolved oxygen

Bottom: ↑nutrients, ↓ dissolved oxygen

Feb

Mar

Apr

almost all year, at all depths. Driving factors controlling Cyanobacteria have been persistently studied, since the 1970s, initiated by the importance of this algal group in eutrophic waters (Shapiro, 1973, 1990; Schindler, 1974; Smith, 1983, 2003; Huszar et al., 2000). Several cyanobacterial species form blooms thus preventing the recreational use or drinking water supply (Branco & Senna, 1996; Beyruth, 2000). Cyanobacterial blooms are commonly related to high temperatures, high pH, low CO2, high P concentration and water column stability, low TN:TP ratio, and grazing pressure (Smith, 1983; Paerl, 1988; Marinho & Huszar, 2002). All conditions above were detected in the Garças Pond: the Spearman Rank Correlation between cyanobacterial biomass and abiotic factors fit the existing literature. Phytoplankton seasonal variation was characterized by shifts in the cyanobacterial species. Phases 1, 2, and 3 defined from abiotic data (see abiotic results) were consistent with phytoplankton community data, supporting the applicability of the functional group (Reynolds et al., 2002) concept in describing seasonal variation of Garças Pond phytoplankton as shown by the CCA. During phase 1 (November–March), there was a marked dominance of Raphidiospis/Cylindrospermopsis (S-group). From April to August (phase 2), Raphidiospis/Cylindrospermopsis density gradually decreased and a more diverse community established with co-existence of some cyanobacterial species (groups K, LM, and M), diatoms (group D) and chlorophytes (groups P and X1). Phase 3 was characterised by Sphaerocavum brasiliense bloom (group M). The summary sequence of functional groups over

May

Jun

Jul

Phase 1



Surface: ↑ pH, chlo-a, TP

Bottom: ↑nutrients, ↓ dissolved oxygen

Cyano( M)

Cyano ( S, H1) Eugleno (W1, W2 ) Crypto (Y)

Cyano ( K, M, Lm), Bacillario (D) Chloro (X1, P, F ) Dino (Lo)

Cyano ( S, H1) Eugleno (W1, W2 ) Crypto (Y)

Jan

Phase 3

Phase 2

Phase1

Aug

Sep

Oct

Nov

Dec

phases 1, 2, and 3 resulted from CCA is: S/W1/W2/ H1/Y ? K/LM/LO/D/P/X1/F ? M (Fig. 8). Thus study indicated S. brasiliense as a key species in Garças phytoplankton community during 1997. It was among the most frequent species and reached the highest relative dominance. It outcompeted other taxa during the September, and influenced the diversity patterns over the year. The genus Sphaerocavum was proposed by Azevedo & Sant’Anna (2003) from samples collected from the Saõ Paulo state eutrophic reservoirs, including the Garças Pond. Since then, S. brasiliense was reported for eutrophic lakes all over the world (Wood et al., 2005; Vardaka et al., 2006). Morphology of Sphaerocavum colonies is very similar to that of Microcystis except for their hollow interior, a consequence of the cell division in two planes. Microcystis aeruginosa is one of the most cited species in Brazilian eutrophic reservoirs (Santos & Calijuri, 1998; Figueredo & Giani, 2001; Marinho & Huszar, 2002) and was described as the most important species in the Garças Pond phytoplankton community in several previous studies, being responsible for regular spring/summer blooms (Sant’Anna et al., 1997; Bicudo et al., 1999). According to this study, Sphaerocavum brasiliense was the main species during phase 3 bloom, replacing M. aeruginosa cited in previous articles. Sphaerocavum and Microcystis have similar ecological requirements. Reynolds et al. (2002) placed both in M group because they form large colonies with biovolume [106 lm3, and their buoyancy control accommodates diel fluctuations during stratifications and mixings in low-latitude lakes. Microcystis panniformis, another significant species

123

278

from Garças Pond phytoplankton community, also belongs to this group that comprises many overlapping taxa and ecotypes. In Garças Pond, it is possible to infer that thermal stratification was the driving factor triggering other water physical and chemical characteristics related to Sphaerocavum brasiliense dominance. Biovolume of S. brasiliense individuals showed great variation over the year, from frequent 2.7 9 103 lm3 (GALD = 26 lm) individuals during phases 1 and 2 to the extreme values of up to 2.4 9 105 lm3 (GALD = 314 lm) during phase 3. Certainly, with moderate turbulence large colonies remain buoyant. During the bloom, pH increased reflecting high photosynthetic rates, and nutrients as NO3 and NO2 that were relatively abundant during the phase 2 were quickly exhausted leading to low NT:TP ratios. S. brasiliense morphological plasticity allowed the species to maintain its population in the Garças Pond all year round, notwithstanding its variations in relative contribution for total biovolume during the three phases. Role of phytoplankton morphological and physiological plasticity in maintaining the (apparently) same populations under different environmental conditions has been thoroughly discussed in recent literature (Naselli-Flores & Barone, 2003; NaselliFlores et al., 2007; Stoyneva et al., 2007; Dokulil et al., 2007). According to Naselli-Flores et al. (2007), morphological variability is recognizable both at population and assemblage level. The same population is maintained when the extent of environmental parameter does not exceed the morphological adaptative capacity of that single population; if environmental changes are strong enough, species replacement takes place offering further adaptation at a higher organization level. During phase 1, Raphidiospis/Cylindrospermopsis was the most important taxon. Raphidiopsis mediterranea and Cylindrospermopsis raciborskii are two very similar species in terms of morphology. According to current literature (Mohamed, 2007), Raphidiopsis mediterranea filaments are sharply pointed at both ends and it never forms heterocytes. Cylindrospermopis raciborskii usually has conically rounded trichome ends and forms heterocytes (Branco & Senna, 1991). Specimens in the Garças Pond had straight trichomes, terminal cells gradually narrowed into almost hair-like appearance. Akinetes

123


were sometimes observed near the thichome ends and heterocytes have not been seen. Raphidiopsis mediterranea was first reported for the Garças Pond by Sant’Anna et al. (1997) in samples collected in 1991–1992. At that time, higher R. mediterranea abundance was detected during the summer, as in the present work. Cylindrospermopsis raciborskii was reported first for the Garças Pond in samples collected also in 1997 by R. C. Gentil (unpublished Master Degree thesis dating from 2000), who reported very few trichomes with heterocytes. Individuals presenting this study corresponded to Raphidiopsis mediterranea’s morphological description. Nevertheless, Cylindrospermopsis raciborskii was confirmed as a key species in the pond since 1998, frequently overwhelming Sphaerocavum and Microcystis during the seasonal fluctuation (Tucci & Sant’Anna, 2003; Crossetti, 2006). For this reason, we used the expression Raphidiopsis/Cylindrospermopsis in this study. Most likely, the year 1997 was a transitional year in the Garças Pond when the preceding Raphidiopsis mediterranea dominance was replaced by Cylindrospermopsis raciborskii. Mohamed (2007) reported about simultaneous occurrence of Raphidiopsis mediterranea and Cylindrospermopsis raciborskii in an Egyptian subtropical shallow pond where their populations were morphologically distinct. Morphology of Raphidiopsis mediterranea corresponded to the descriptions and Cylindrospermopsis raciborskii filaments were coiled with heterocytes at one or both ends. The same author reported also about differences in their toxicity but genetic studies to distinguish the two species have never been carried out. Although information about C. raciborskii ecology is abundant (Padisa´k, 1997; Isvańovics et al., 2000; Bouvy et al., 2003; Tucci & Sant’Anna, 2003), R. mediterranea has lesser reports. According to McGregor & Fabbro (2000), sufficient evidence accumulated for considering Raphidiopsis-like trichomes as environmental morphotypes of Cylindrospermopsis raciborskii. Such suggestion was also raised by Cronberg (1977) based on observations in Brazilian reservoirs. She found that R. mediterranea trichomes can be triggered to form heterocytes after P or sewage water addition. Life cycle of Cylindrospermopsis raciborskii confuses further the picture: freshly germinated filaments are very much similar to filaments of Raphidiopsis mediterranea (Singh, 1962; Padisa´k, 2003).


Brazilian C. raciborskii populations typically show some 10% of heterocyte bearing individuals (Branco & Senna, 1996; Huszar et al., 2000). Tucci & Sant’Anna (2003) reported\9% of specimens with heterocytes from Garças Pond. According to Padisa´k & Reynolds (1998), C. raciborskii could be considered a ‘heterocytic Oscillatoria’ equipped with numerous ecological adaptations that will turn the species into a very successful competitor in Nature. Although C. raciborskii is a N-fixer, it does not seem to be highly dependent on N fixation, preferring ´ k, 1997). NH+4 –NO3 as N source (Padisa Heterocytic cyanobacterial dominance is commonly reported under low availability of inorganic N (for example, NO3-N:TP ratio \ 5; McQueen & Lean, 1987). In Garças Pond, smaller NO3 concentrations coincided with high cyanobacterial biomass, including non-heterocytic species such as Sphaerocavum brasiliense in September (phase 3) and the summer period (phase 1). During this study, only Anabaena planctonica specimens possessed heterocytes in \10% of samples. Ecological characteristics of Cylindrospermopsis raciborskii and Raphidiopsis mediterranea populations were found to be similar by Mohamed (2007). In this study, the two species were positively associated, but negatively correlated with Microcystis aeruginosa and both declined when water temperature fall below 17°C. These patterns are very much like the observations made in the Garças Pond. The following explanation is proposed for the M ? S succession between phases 3 and 1: September usually characterized by warm and dry weather in the Garças Pond area, a condition that allows development of stratifications that establishes after some months of complete mixing (winter), when nutrients were homogeneously distributed along the entire water column. Although Sphaerocavum brasiliense perennial, stratification, and nutrient abundancy allow development of large colonies in September exhausting nutrients from the epilimnion. Stratification prevailed during summer months (phase 1) and Raphidiopsis/Cylindrospermopsis, as a very efficient nutrient uptaker and light-collector took advantage, being able to develop great densities during phase 1. Discontinuous mixing events probably happened during phase 1, but were not pronounced enough to result in homogenous profiles. Another possible explanation for the M group

279

decrease during phase 1 might be that increased precipitation induces turbulences that inhibit maintenance of large colonies. Acknowledgments BMF thanks to FAPESP (Fundaçaõ de Amparo a` Pesquisa do Estado de Saõ Paulo) for a Doctoral fellowship, and CEMB to CNPq (Conselho Nacional de Desenvolvimento Cientı´fico e Tecnolo´gico) for Grant n° 303876/2004-2. Both authors are thankful to all colleagues involved in the laboratory and fieldwork, and to Dr. Denise de Campos Bicudo for fruitful discussions. BMF and CEMB are also very grateful to Dr. Jirˇi Koma´rek for his comments on Raphidiopsis/Cylindrospermopsis taxonomic definitions, and to two anonymous referees for their excellent contributions.

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