PRIMARY RESEARCH PAPER

Phytoplankton seasonal variation in a shallow stratifiedeutrophic reservoir (Garcas Pond, Brazil)

Barbara 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

� Springer Science+Business Media B.V. 2007

Abstract This study aimed at describing the

phytoplankton dynamics and structure in a shallow

eutrophic reservoir, the Garcas Pond, located in the

Parque Estadual das Fontes do Ipiranga (23�38040.600

S, 46�37028.000 W), in the Municipality of Sao 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. Phyto-

plankton seasonal and vertical variation was related

to shifts in the water chemical features as a conse-

quence 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

were shifts in cyanobacterial dominance over the

entire year. During phase 1, Raphidiopsis/Cylindro-

spermopsis 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

CO32- concentration reached their highest values.

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 metabo-

lism was frequently addressed (Scheffer, 1998;

Scheffer & van Nes, 2007). Their responses to

eutrophication can be catastrophic, mainly due to

Handling editor: J. Padisak

B. M. Fonseca (&)

Curso de Ciencias Biologicas, Universidade Catolica

de Brasılia, QS 07, Lote 1, Aguas Claras, Brasilia, DF

71966-700, Brazil

e-mail: bm_fonseca@yahoo.com.br

C. E. de M. Bicudo

Instituto de Botanica, Secao de Ecologia, Caixa postal

3005, Sao Paulo, SP 01061-970, Brazil

123

Hydrobiologia (2008) 600:267–282

DOI 10.1007/s10750-007-9240-9

the intense water–sediment interaction (Bicudo et al.,

2007). Padisak & 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, phyto-

plankton 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 estab-

lishment of predictive models applied to natural

communities (Reynolds, 2006). An increasing num-

ber of authors have emphasized species’ morpho-

functional attributes as important tools in phyto-

plankton dynamics studies (Huszar & Caraco, 1998;

Reynolds et al., 2002; Salmaso & Padisak, 2007).

Many studies described temporal phytoplankton

patterns in lakes with varying mixing regimes.

These include functional shallow lakes such as

Balaton (Zmax = 11 m; Padisak, 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; Mor-

abito et al., 2003). Notwithstanding, this matter is

far from being exhausted. Accelerated rates of

anthropogenic eutrophication are continuously

demanding management strategies applied to eutro-

phic reservoirs, with particular emphasis to those in

tropical countries.

In Brazil, phytoplankton communities from eutro-

phic 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

incident, when people died as a consequence of liver

failure caused by microcystin toxin from cyanobac-

terial blooms (Komarek et al., 2001).

Garcas Pond phytoplankton was already described

from various aspects like taxonomy (Azevedo &

Sant’Anna, 1999, 2003; Komarek & Azevedo, 2000;

Tucci et al., 2006), ecology (Sant’Anna et al., 1989,

1997; Ramırez & Bicudo, 2002; Tucci, 2002; Tucci

& Sant’Anna, 2003; Fonseca, 2005; Ramırez &

Bicudo, 2005; Crossetti & Bicudo, 2005a, b; Cros-

setti, 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 mecha-

nisms underlying limnological variations in the

reservior during the period 1997–2004.

Present article aims at describing the phytoplank-

ton seasonal and vertical variation in the Garcas

Pond, with emphasis on its dynamics and structure

before the water hyacinth proliferation and in relation

to the abiotic environment.

Study area

Garcas Pond (23�38040.600 S, 46�37028.000 W) is

located in the Parque Estadual das Fontes do Ipiranga

Biological Reserve (PEFI; 526 ha; 798 m.a.s.l) situ-

ated in the Municipality of Sao 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–Febru-

ary) 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 Garcas 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). Garcas Pond has

one outlet and seven tributaries, four of which carring

sewage (Henry et al., 2004).

268 Hydrobiologia (2008) 600:267–282

123

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 (Gol-

terman & Clymo, 1971), free CO2, HCO3- and CO3

2-

(Mackereth et al., 1978), DO (Golterman et al., 1978),

NH4+ (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. NH4+–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 Utermohl

(1958). Sedimentation time followed Lund et al.

(1958). The number of settling units counted in each

individual sample varied according to species accu-

mulation curve. The same chamber volume (2 ml)

was used throughout the year and at least 40 fields

were counted for each chamber (Rott, 1981). Biovo-

lume 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 as dominant. Shannon-Wiener Index

(H0 ¼ �P½pi log2 pi�) was used to estimate diver-

sity (Shannon & Weaver, 1949).

Spearman Rank Correlation was used to test

association between abiotic and biotic variables.

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 corre-

spondence 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, biological data were transformed by

½ffiffiffiffiffiffiffiffiffiffiffiffiffiffiffixþ 0:5p

� 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 sig-

nificant 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, NH4+, 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, NH4+ 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

Hydrobiologia (2008) 600:267–282 269

123

RTR0 10 20 30 40

)m( htpe

D

0

1

2

3

4

Temperature (°C)16 18 20 22 24

O2 (mg.L-1)0 2 4 6 8 10

Jan

Temperature (°C)16 18 20 22 24

)m( htpe

D

0

1

2

3

4

O2 (mg.L-1)0 2 4 6 8 10

RTR0 10 20 30 40

Feb

Temperature (°C)16 18 20 22 24

)m( htpe

D

0

1

2

3

4

O2 (mg.L-1)0 2 4 6 8 10

RTR0 10 20 30 40

Mar

Temperature (°C)16 18 20 22 24

)m( htpe

D

0

1

2

3

4

O2 (mg.L-1)0 2 4 6 8 10

RTR0 10 20 30 40

Apr

Temperature (°C)16 18 20 22 24

)m( htpe

D

0

1

2

3

4

O2 (mg.L-1)0 2 4 6 8 10

RTR0 10 20 30 40

May

Temperature (°C)16 18 20 22 24

)m( htpe

D

0

1

2

3

4

O2 (mg.L-1)0 2 4 6 8 10

RTR0 10 20 30 40

Jun

Temperature (°C)16 18 20 22 24

)m( htpe

D

0

1

2

3

4

O2 (mg.L-1)0 2 4 6 8 10

RTR0 10 20 30 40

Jul

RTR0 10 20 30 40

)m( htpe

D

0

1

2

3

4

Temperature ( °C)16 18 20 22 24

O2 (mg.L-1)0 2 4 6 8 10

Aug

Temperature (°C)16 18 20 22 24

)m( htpe

D

0

1

2

3

4

O2 (mg.L-1)0 2 4 6 8 10

RTR0 10 20 30 40

Sep

Temperature (°C)16 18 20 22 24

)m( htpe

D

0

1

2

3

4

O2 (mg.L-1)0 2 4 6 8 10

RTR0 10 20 30 40

Oct

Temperature (°C)16 18 20 22 24

)m( htpe

D

0

1

2

3

4

O2 (mg.L-1)0 2 4 6 8 10

RTR0

Nov

Temperature (°C)16 18 20 22 24

)m( htpe

D

0

1

2

3

4

O2 (mg.L-1)0 2 4 6 8 10

RTR0 10 20 30 40

Dec

Temperature RTRDissolved oxygen Zmix

10 20 30 40 50 60

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

270 Hydrobiologia (2008) 600:267–282

123

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

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 Garcas 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 (subsur-

face, 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, NH4+, free CO2, conductivity, DO,

D

epth

(m

)

Dep

th (

m)

D

epth

(m

)

Dep

th (

m)

Dep

th (

m)

Dep

th (

m)

S

1

6282102122142162182202222242

2

3

B

)1-L g

u( or

ush

psohp lato

T

S

1

15011502150315041505150615071508150915010150111501215013150

2

3

B

Tni

trog

en lato

)1-L gu(

S

1

481216202428323640

2

3

B

SR

u( P

g)1-

L

S

1

2001400260038005000620074008600980011000

2

3

B Am

mon

ium

) 1-

L gu(

S

1

2939495969798999109119129

2

3

B

m( 2O

C latoT

g)1-

L

Month

S

1

Jan868128188248308368428488

2

3

B

Feb Mar Apr May Jul Aug Sep Oct Nov Dec

)1-L.gu( etar ti

N

Phase 1 Phase 2 Phase 3 Phase 1

Jun

(a)

(b)

(c)

(d)

(e)

(f)

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 Garcas Pond during 1997. Temporal

phases are indicated by vertical lines

Table 1 Mean values of water variables in Garcas 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

Total CO2 (mg l-1) 57.9 36.8 37.4

Free CO2 (mg l-1) 16.1 9.0 4.4

HCO3- (mg l-1) 57.9 38.5 45.2

CO32- (mg l-1) 0.022 0.013 0.455

N–NH4+ (lg l-1) 2,957.6 1,209.3 2,052.3

N–NO2- (lg l-1) 22.2 27.9 \5.0

N–NO3- (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) 1,166.2 668.3 226.6

SRP (lg l-1) 7.1 \4.0 7.1

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 (mm3 l-1) 18.3 20.6 67.4

Density (ind ml-1) 12,173 9,763 5,720

Hydrobiologia (2008) 600:267–282 271

123

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

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, NH4+, free CO2, and conduc-

tivity 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

NO2- values. Phase 3 samples were associated to high

TP and pH values on the opposing side and phase 1

samples grouped at the central part of the graph.

Biotic variables

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 Cyano-

bacteria and Euglenophyceae (29 taxa each). The

most frequent taxa were: Chlorella vulgaris, Trache-

lomonas volvocinopsis, Merismopedia glauca,

06

12

1824303642

485460

oitar ralom

PT:

NT

0200400600800

100012001400160018002000

Jan

Month

oitar ralom

PRS:

NID

Phase 1 Phase 2 Phase 3 Phase 1

1 m 2 m Subsurface

Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec

(a)

(b)

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 Garcas Pond. Temporal phases are indicated

by vertical lines

ja

fe

mr

ap

ma

jn

jl

au

se

oc

no

de

ja

femr

ap

ma

jn

jl

au

se

oc

no

de

ja

femrap

ma

jn

jl

au

se

oc

no

de

ja

fe

mr

ap

ma

jn

jl

au

se

oc no

de

ja

fe

mrap

ma

jn jl

au

se

oc

node

pH

cond

turb

DO

NO2

NO3

NH4

TN

SRPPDT

TP

SiCO2

chlo-a

-1,0

-1,5

0,0 1,0 2,0

-0,5

0,5

Axis 1 (36%)

)% 32( 2 si x

A

Depths

Subsurface1 m2 m3 mBottom

Phase 1

Phase 3

Phase 2

Surface Bottom

Fig. 4 Biplot of PCA

for abiotic variables. Two

letters in sample unit

plots represent month

(ja = January,

fe = February, etc.)

272 Hydrobiologia (2008) 600:267–282

123

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

0%

20%

40%

60%

80%

100%

0%

20%

40%

60%

80%

100%

Jan

Cyanophyceae Dinophyceae CryptophyceaeEuglenophyceae Chlorophyceae BacillariophyceaeOthers

Subsurface

Bottom

Feb Mar Apr May Jun Jul Ago Sep Oct Nov Dec

Fig. 5 Seasonal and vertical variation of phytoplankton

taxonomic classes relative contribution to total biovolume in

the Garcas Pond during 1997. To save space, just subsurface

and bottom data are shown

Dep

th (

m)

Dep

th (

m)

Dep

th (

m)

S

1

081624324048566472808896104112120128136144

2

3

B

biov

olum

e l ato

T( m

m)1-

L 3

S

1

081624324048566472808896104112120128136144

2

3

B

. bra

silie

nse

S( m

m)1 -

L 3

Month

S

1

Jan

0123456789101112

2

3

B

Feb May Jul Sep Oct Nov

R( nily

C/ h pam

m)1 -

L 3

Phase 1 Phase 2 Phase 3 Phase 1

Mar Apr Jun Aug Dec

(a)

(b)

(c)

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)

Hydrobiologia (2008) 600:267–282 273

123

Table 2 Selected species from Garcas 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 Group (%)

1 2 3

Microcystis aeruginosa (Kutzing) Kutzing M 43.6 50.2 93.0

M. panniformis Komarek et al.

Sphaerocavum brasiliense Azevedo & Sant’Anna

Raphidiopsis/Cylindrospermopsis S 16.1 7.5 0.2

Geitlerinema unigranulatum (Singh) Komarek & Azevedo

Planktothrix agardhii (Gomont) Komarek & Anagnostidis

Anabaena planctonica Brunnthaler H1 0.6 0.1 0.0

Aphanocapsa elachista West & West K 0.7 6.3 1.2

A. incerta (Lemmermann) Cronberg & Komarek

Cyanodictyon sp. 1

Merismopedia glauca (Ehrengerg) Kutzing Lo 1.6 0.3 0.5

M. tenuissima Lemmermann

Gymnodinium sp. 1 LM 7.5 13.0 0.4

Peridinium cinctum (Muller) Ehrenberg

Peridinium willei Huitfeld-Kaas

Ulnaria acus (Kutzing) M. Aboal D 0.5 2.9 0.0

Fragilaria rumpens (Kutzing) G. W. F. Carlson

Botryococcus braunii Kutzing F 0.8 0.3 0.4

Closteriopsis acicularis (G. M. Smith) Belch & Swale P 4.0 0.4 0.3

Closterium gracile Brebisson ex Ralfs

Euglena acus Ehrenberg W1 3.4 0.2 0.0

E. proxima Dangeard

E. splendens Dangeard

Trachelomonas hispida (Perty) Stein emend. Deflandre W2 7.0 2.6 0.8

T. kellogii Skvortzov emend. Deflandre

T. volvocinopsis Swirenko

Cryptomonas curvata Ehrenberg emend. Penard Y 8.7 6.5 0.5

C. erosa Ehrenberg

C. marssonii Skuja

Ankistrodesmus gracilis Corda sensu Korsikov X1 0.8 0.2 0.0

Chlorella vulgaris Beijerinck

Chlorococcum infusionum (Schrank) Meneghini

Crucigenia tetrapedia (Kirchner) West & West

Micractinium pusillum Fresenius

Monoraphidium contortum (Thuret in Brbisson)

Pseudodidymocystis fina ((Komarek) Hegewald & Deason)

Scenedesmus ecornis (Ehrenberg) Chodat

274 Hydrobiologia (2008) 600:267–282

123

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

Garcas 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 nega-

tively 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

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 environ-

ment-species correlation for the two significant

axes was high ([0.7) (0.864 and 0.754, respec-

tively), 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 condi-

tions. 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 concentra-

tions. 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 Axis 2

Canonical coeficient 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

Correlation coefficient

(intra-set)

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

Hydrobiologia (2008) 600:267–282 275

123

Discussion

Similarly to temperate lakes, tropical ones also may

experience seasonal climatic variations that deter-

mine 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 temper-

ature and dry weather. This pattern is described for

many aquatic environments in the Southern Hemi-

sphere (Ashton, 1985). The lowest air temperatures

during coldest months led to an increase of water

density allowing complete mixing of Garcas Pond.

During the warm-wet spring/summer period, how-

ever, high water temperatures resulted in relatively

stable water column stratification.

Despite the shallowness of the Garcas Pond, it was

persistently stratified for a few weeks during the

spring and summer like a typical discontinuous

polymictic reservoir (Ramırez & Bicudo, 2002). A

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 varia-

tion. Similar results have been reported for Ninfeias

Pond, which is shallower than 5 m and located in

\1 km distance from Garcas one (Fonseca, 2005).

According to Padisak & 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,

Garcas 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 Garcas Pond only

during phase 2.

Cyanobacteria dominated the Garcas Pond phyto-

plankton community with [50% of total biomass

MH1S

KLoLmDF

P

W1W2 Y

X1

pH

TP

free CO2

temp

DIN

-2

-2,0

0 2

-1,0

0,0

1,0

2,0

Axis 1

2 sixA

Phases

123

Phase 1 Phase 2 Phase 3

Stratification

Mixing

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 Garcas Pond during

1997 (n = 36)

276 Hydrobiologia (2008) 600:267–282

123

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 Garcas Pond: the Spearman Rank

Correlation between cyanobacterial biomass and

abiotic factors fit the existing literature.

Phytoplankton seasonal variation was character-

ized 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 sea-

sonal variation of Garcas Pond phytoplankton as

shown by the CCA.

During phase 1 (November–March), there was a

marked dominance of Raphidiospis/Cylindrosperm-

opsis (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 charac-

terised by Sphaerocavum brasiliense bloom (group

M). The summary sequence of functional groups over

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 Garcas phytoplankton community during

1997. It was among the most frequent species and

reached the highest relative dominance. It outcom-

peted other taxa during the September, and influenced

the diversity patterns over the year.

The genus Sphaerocavum was proposed by Azev-

edo & Sant’Anna (2003) from samples collected from

the Sao Paulo state eutrophic reservoirs, including the

Garcas Pond. Since then, S. brasiliense was reported

for eutrophic lakes all over the world (Wood et al.,

2005; Vardaka et al., 2006). Morphology of Sphaer-

ocavum 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 Garcas Pond phytoplankton

community in several previous studies, being respon-

sible for regular spring/summer blooms (Sant’Anna

et al., 1997; Bicudo et al., 1999). According to this

study, Sphaerocavum brasiliense was the main spe-

cies during phase 3 bloom, replacing M. aeruginosa

cited in previous articles.

Sphaerocavum and Microcystis have similar eco-

logical 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 strat-

ifications and mixings in low-latitude lakes.

Microcystis panniformis, another significant species

Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec

Phase1 Phase 2 Phase 1Phase 3

↑ Temperature

Stratification

⇓Bottom: ↑nutrients,

↓ dissolved oxygen

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

Crypto (Y)

↓ Temperature

Mixing

⇓↓ nutrients

↑ dissolved oxygen

Cyano (K, M, Lm),Bacillario (D)

Chloro (X1, P, F )Dino (Lo)

↑ Temperature

Stratification

⇓Bottom: ↑nutrients,

↓ dissolved oxygen

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

Crypto (Y)

↑ Temperature

Stratification

⇓Surface: ↑ pH,

chlo-a, TP

Cyano( M)

Fig. 8 Synthesis diagram

showing main abiotic and

biological changes during

the year 1997 in the Garcas

Pond

Hydrobiologia (2008) 600:267–282 277

123

from Garcas Pond phytoplankton community, also

belongs to this group that comprises many overlap-

ping taxa and ecotypes.

In Garcas 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 Garcas

Pond all year round, notwithstanding its variations

in relative contribution for total biovolume during

the three phases.

Role of phytoplankton morphological and physi-

ological plasticity in maintaining the (apparently)

same populations under different environmental con-

ditions has been thoroughly discussed in recent

literature (Naselli-Flores & Barone, 2003; Naselli-

Flores 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 environ-

mental 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 mediter-

ranea and Cylindrospermopsis raciborskii are two

very similar species in terms of morphology. Accord-

ing 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 Garcas

Pond had straight trichomes, terminal cells gradually

narrowed into almost hair-like appearance. Akinetes

were sometimes observed near the thichome ends and

heterocytes have not been seen.

Raphidiopsis mediterranea was first reported for

the Garcas 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 Garcas Pond in

samples collected also in 1997 by R. C. Gentil

(unpublished Master Degree thesis dating from

2000), who reported very few trichomes with hetero-

cytes. Individuals presenting this study corresponded

to Raphidiopsis mediterranea’s morphological

description. Nevertheless, Cylindrospermopsis raci-

borskii 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/Cylindrosperm-

opsis in this study. Most likely, the year 1997 was a

transitional year in the Garcas Pond when the preced-

ing Raphidiopsis mediterranea dominance was

replaced by Cylindrospermopsis raciborskii.

Mohamed (2007) reported about simultaneous

occurrence of Raphidiopsis mediterranea and Cylin-

drospermopsis raciborskii in an Egyptian subtropical

shallow pond where their populations were morpho-

logically 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 (Padisak, 1997;

Isvanovics et al., 2000; Bouvy et al., 2003; Tucci &

Sant’Anna, 2003), R. mediterranea has lesser reports.

According to McGregor & Fabbro (2000), suffi-

cient evidence accumulated for considering

Raphidiopsis-like trichomes as environmental mor-

photypes 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 con-

fuses further the picture: freshly germinated filaments

are very much similar to filaments of Raphidiopsis

mediterranea (Singh, 1962; Padisak, 2003).

278 Hydrobiologia (2008) 600:267–282

123

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 Garcas Pond. According to Padisak

& Reynolds (1998), C. raciborskii could be consid-

ered 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

NH4+–NO3

- as N source (Padisak, 1997).

Heterocytic cyanobacterial dominance is com-

monly reported under low availability of inorganic

N (for example, NO3-N:TP ratio \ 5; McQueen &

Lean, 1987). In Garcas Pond, smaller NO3- concen-

trations coincided with high cyanobacterial biomass,

including non-heterocytic species such as Sphaer-

ocavum brasiliense in September (phase 3) and the

summer period (phase 1). During this study, only

Anabaena planctonica specimens possessed hetero-

cytes in \10% of samples.

Ecological characteristics of Cylindrospermopsis

raciborskii and Raphidiopsis mediterranea popula-

tions 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 tempera-

ture fall below 17�C. These patterns are very much

like the observations made in the Garcas Pond.

The following explanation is proposed for the

M ? S succession between phases 3 and 1: Septem-

ber usually characterized by warm and dry weather in

the Garcas 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 bra-

siliense 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 prob-

ably happened during phase 1, but were not

pronounced enough to result in homogenous profiles.

Another possible explanation for the M group

decrease during phase 1 might be that increased

precipitation induces turbulences that inhibit mainte-

nance of large colonies.

Acknowledgments BMF thanks to FAPESP (Fundacao de

Amparo a Pesquisa do Estado de Sao Paulo) for a Doctoral

fellowship, and CEMB to CNPq (Conselho Nacional de

Desenvolvimento Cientıfico e Tecnologico) 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. Jiri Komarek for his comments on

Raphidiopsis/Cylindrospermopsis taxonomic definitions, and

to two anonymous referees for their excellent contributions.

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