Freshwater Biology (2008) 53, 952–963 doi:10.1111/j.1365-2427.2008.01957.

Phytoplankton equilibrium phases during thermal

stratification in a deep subtropical reservoir
V A N E S S A B E C K E R * , V E R A L Ú C I A M . H U S Z A R * , L U I G I N A S E L L I - F L O R E S †
A N D J U D I T P A D I S Á K ‡
*Laboratory of Phycology, National Museum of Rio de Janeiro, Federal University of Rio de Janeiro, Rio de Janeiro, Brazil
†
Department of Botanical Sciences, University of Palermo, Palermo, Italy
‡
Department of Limnology, University of Pannonia, Egyetem, Hungary

SU M M A R Y
1. Equilibrium and non-equilibrium hypotheses have often been used to explain
observations in community ecology. Published case studies have demonstrated that steady
state phytoplankton assemblages are more likely to occur in deep lakes than in shallow
mixed ones.
2. Phytoplankton seasonal succession was studied by weekly sampling in Faxinal
Reservoir (S Brazil), a subtropical deep, clear, warm monomictic and slightly eutrophic
reservoir. This study demonstrated an alternation of steady and non-steady state phases of
phytoplankton assemblages with different dominant species during the steady states.
3. During the studied period, three steady states were identified with different dominant
algal species: Anabaena crassa (Cyanobacteria), Nephrocytium sp. (green algae) and
Asterionella (diatoms).
4. Each steady state in Faxinal Reservoir developed under stratified conditions of the water
column according to the predictions of the disturbance concepts. Apparently, the major
forces driving the development and persistence of these steady-state phases were closely
related to thermal stratification and its consequences.
5. This study is the first report on development of more than one steady state within a year
in a stratified water body. The development of three steady states might be the result of the
relatively long stratification period in the Faxinal Reservoir and to its unique geochemical
features.

Keywords: Brazil, equilibrium phase, monomictic reservoir, steady state

as a result of higher growth rates and competition

Introduction
between species becomes important (equilibrium).
Equilibrium and non-equilibrium viewpoints may Equilibrium and non-equilibrium hypotheses have
simply be considered as two ends of an ecological often been used to explain community ecology. Steady
spectrum (Harris, 1986). In unstable environments, state conditions are expected to be more likely to
growth rates may be reduced and populations are occur in deep lakes than in shallow mixed ones
limited by environmental factors (non-equilibrium). (Mischke & Nixdorf, 2003). Most reported phyto-
In more stable environments, population size may rise plankton steady-states have been related to stratified
conditions (Dokulil & Teubner, 2003; Leitão et al.,
Correspondence: Vanessa Becker, Laboratory of Phycology, 2003; Morabito, Oggioni & Panzani, 2003).
National Museum of Rio de Janeiro, Federal University of Rio de In natural phytoplankton communities, it is often
Janeiro, Quinta da Boa Vista s ⁄ no, São Cristovão, Rio de Janeiro, difficult to determine whether a given ‘phase’ in a
20940-040, Brazil. E-mail: becker.vs@gmail.com seasonal sequence can be considered to be in
952  2008 The Authors, Journal compilation  2008 Blackwell Publishing Ltd
 Phytoplankton equilibrium phases 953
equilibrium or not, due to a lack of chemical data probable and longer lasting in tropical (Ganf, 1974;
and ⁄ or to insufficient sampling frequency (Sommer Rott, 2002) and polar region (Allende & Izaguirre,
et al., 1993). Constancy of biomass is needed as a 2003) because seasonal changes vary over a narrower
measure of functional persistence of the ecosystem range and at least one season is considerably longer
(top-down and bottom-up controls are probably than the others.
equilibrated or bottom-up dominates; Padisák et al., In this paper, we analyse the weekly changes of
2003a). A maximum of three species contributing to at phytoplankton composition and biomass in a sub-
least 80% of total biomass for more than 2 weeks, tropical, eutrophic, monomictic reservoir in order to
without considerable variation in total biomass, has identify equilibrium phases, according to the defini-
been proposed as a criterion to identify an equilib- tion given by Sommer et al. (1993). These phases are
rium phase (Sommer et al., 1993). generally expected during thermal stratification when
Ecologists have quite different opinions about the disturbance is weaker and progression towards equi-
importance of competition in shaping diversity. For librium is likely to occur.
example, Harris (1986) assumes that competition
contributes to the generation of diversity over evolu-
tionary time scales but it may not be necessary to Methods
invoke competition as a mechanism to explain the
Study site
maintenance of diversity over ecological time scales.
In Connell’s (1978), intermediate disturbance hypoth- Faxinal Reservoir (2905¢00¢¢S; 5103¢30¢¢W) is the main
eses competitive exclusion is the major mechanism water supply system of Caxias do Sul City (400 000
that results in low diversity and the latter has been inhabitants), in the south of Brazil (Fig. 1). It has a
supported by theoretical models (Tilman, 1977), lab- surface area of 3.1 km2 at 700 m a.s.l. The Reservoir is
oratory experiments (Sommer, 1985) and field studies deep (zmax = 30 m), warm monomictic and eutrophic
(see a selection of papers in Padisák, Reynolds & (TP 29.4 lg L)1 and chlorophyll a 15 lg L)1 – epilim-
Sommer, 1993). nion annual mean). The regional climate is temperate
Nevertheless, equilibrium theory takes one extreme without a dry season (Cfa type; Köppen, 1936) with an
viewpoint: competition was acting, is acting, and will average annual temperature of 16 C and precipita-
always be acting (Harris, 1986). Steady state is a tion between 1800 and 2200 mm.
dynamic equilibrium as losses and gains are acting
through time, and result in a relative invariance of the
Sampling
assemblage. Moreover, the mechanisms controlling
steady-state phytoplankton assemblages would be The criteria for sampling were based on those set by the
competition, and ⁄ or trophic relationships and ⁄ or bio- Water Company sampling protocol: weekly algal
geochemical processes, and so on. Many other selec- monitoring (at the surface) and monthly nutrient
tive forces (grazing, allelopathy, bloom from a bank of analyses in the Faxinal Reservoir, in the water intake
resting stages, invasions, parasitism, etc.) in a complex sampling station (Fig. 1) since 2002. Although this
aquatic system could be acting simultaneously, or sampling frequency was set to be sufficient for man-
alternately, and this may lead to the establishment of a agement needs, it is adequate to follow changes in
steady state (Rojo & Álvarez-Cobelas, 2003). Each phytoplankton composition (Sommer et al. 2003) and
species in non-equilibrium community occupies a its adequacy was supported recently by Monte-Carlo
different niche that results from and reduces direct simulations (Honti, Istvanovics & Osztoics, 2007).
competition and thus species composition is more or Profiles of temperature, dissolved oxygen, pH and
less stable depending on environmental predictability conductivity were measured with a multiparameter
(Whittaker, 1975). probe Horiba (model U-10), at 1 m intervals from the
In temperate-climate phytoplankton, a steady state surface to the bottom. Transparence of the water was
is hard to find (Naselli-Flores et al., 2003). Temperate estimated with a Secchi disk; turbidity (NTU) was
zones are moderately stable in terms of physical and measured with a turbidimeter HACH 2100P.
biological conditions in comparison to other geo- Phytoplankton samples were taken weekly (January
graphical regions. Steady state conditions are more 2004–January 2005) from the surface layer (between 0
 2008 The Authors, Journal compilation  2008 Blackwell Publishing Ltd, Freshwater Biology, 53, 952–963
954 V. Becker et al.

Brazil

Rio Grande
do Sul

29°05’00” S
51°03’30” W
Faxinal

Herval

Alegre N

Faxinal reservoir Scale - 1:50:000 Fig. 1 Faxinal Reservoir showing the

sampling station.

and 0.5 m) at the deepest part of the reservoir with a 400·. Settling units (cells, colonies and filaments) were
Van Dorn bottle (2 L), and they were preserved with enumerated in random fields (Uhelinger, 1964) and at
neutral Lugol¢s iodine solution. least 100 specimens of the most frequent species were
Monthly samples for analyses of inorganic nutrients counted (Lund, Kipling & Lecren, 1958).
were collected at the surface, with a Van Dorn Bottle
(2 L), at a fixed time (09:00 am).
Data analysis
Euphotic zone (zeu) was calculated as 2.7 times the
Sample analysis
Secchi depth (Cole, 1994) and mixing zone (zmix) was
Dissolved inorganic nutrients – soluble reactive phos- estimated from temperature and dissolved oxygen
phorus (SRP), nitrite (NO2-N), nitrate (NO3-N), profiles. The ratio between euphotic and mixing
ammonium (NH4-N) and soluble reactive silicate depths (zeu : zmix) was used as a measure of light
(SRSi) – were analysed in filtered samples (Sartorius availability (Jensen et al., 1994).
membrane cellulose acetate filters; 0.45 lm). SRP and The dimensionless parameter relative water column
NO2-N were measured spectrophotometrically stability (RWCS) was calculated according to Padisák
(Murphy & Riley, 1962; Aminot & Chaussepied, et al. (2003b) by comparing the density difference
1983). NO3-N was measured by flow injection analysis between bottom (Db) and surface (Ds) water to the
using the cadmium reduction method (Wood, Arm- density difference between 4 C (D4) and 5 C (D5) of
strong & Richards, 1967; modified by Aminot & pure water, using the formula:
Chaussepied, 1983), NH4-N by the indophenol spec-
Db  Ds
trophotometric method (Solorzano, 1969; modified by RWCS ¼
D4  D5
Strickland & Parsons, 1972) and SRSi by the molyb-
date method (Mullin & Riley, 1955). Phytoplankton biomass was estimated volumetri-
Phytoplankton was quantitatively analysed with a cally (Edler, 1979; Hillebrand et al., 1999) assuming a
Leica - DMIL inverted microscope (Utermöhl, 1958) at specific gravity of 1 mg mm)3 (Wetzel & Likens, 2000).
 2008 The Authors, Journal compilation  2008 Blackwell Publishing Ltd, Freshwater Biology, 53, 952–963
 Phytoplankton equilibrium phases 955
Steady-state phases were identified according to Som- Results
mer et al. (1993): no more than three coexisting species,
Physicochemistry scenario
contributing more than 80% to the total biomass, for at
least 2 weeks. The Shannon and Wiener function was Temperature profiles allowed us to identify only one
used to measure compositional diversity (Shannon & period of total vertical mixing, which occurred in
Weaver, 1949) from biomass data; evenness was winter (June–August 2004; Fig. 2). Consistently, the
calculated according to Pielou (1966). relative stability of the water column (RWCS) reached
Nonparametric correlation (Spearman) analyses its maximum of 296 in January 2004 (Fig. 3). The
were used to determine relationships among the mixing zone was euphotic during summer and
biomasses of dominant species and the environmental autumn, and the euphotic depth decreased to only
factors (mixing regime, light and nutrients). 60% of the epilimnion during spring (Fig. 4). Turbidity

(a) 0 ºC
3 28.0
26.5
6 25.0
23.5
10
22.0
20.5
15 19.0
17.5
16.0
20
14.5
13.0
25 11.5
10.0

30
(b) 0 %
100
3
90
6
80

10 70
Depth (m)

60
50
15
40
30
20
20
10
25
0

30 –1
µg L
(c) 0
3 36
32
28
10
24
20
16
12
8
4
30 0
Fig. 2 Depth-time isopleths of (a) tem-
perature (ºC); (b) dissolved oxygen (%); J F M A M J J A S O N D J
(c) soluble reactive P (lg L)1) in Faxinal
Reservoir in 2004.
Stratification Mixing Stratification

 2008 The Authors, Journal compilation  2008 Blackwell Publishing Ltd, Freshwater Biology, 53, 952–963
956 V. Becker et al.
was closely related to the mixing regime with high Nutrient dynamics (Table 1) were driven by the
values during the mixing period (Fig. 4). stratification pattern. In particular, SRP showed its
Anoxic conditions were observed from 14 m to the highest values in the first stratification period
bottom of the reservoir only during the first stratifi- (Fig. 2c), probably due to the strong hypolimnetic
cation period. Orthograde oxygen profiles were anoxia. At the same time, dissolved inorganic nitro-
recorded only during the mixing period (Fig. 2). gen (DIN) and SRSi concentrations were low. After
Slightly alkaline conditions characterized the epilim- the vernal overturn, SRP decreased and ammonium
nion during the entire period, with an annual average increased sharply, followed by a similar increase
pH of 7.58 (Fig. 4). in nitrate concentrations that indicated a gradual

350
300
250
RWCS

200
150
100
50
0
J F M A M J J A S O N D J Fig. 3 Seasonal variation of relative water
column stability (RWCS) in Faxinal Res-
Stratification Mixing Stratification ervoir in 2004.

m 10 SS SS Zeu Zmix SS
8

(a) 0

15

12

9
NTU

(b) 0

8
pH

5 Fig. 4 Seasonal variation of: (a) euphotic

zone (shade bar) and mixing zone (black
(c) 4 line), (b) turbidity (NTU) and (c) pH in
Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Jan Faxinal Reservoir in 2004. Shaded areas
(SS) indicating steady states identified by
I II III IV V VI the phytoplankton composition.

 2008 The Authors, Journal compilation  2008 Blackwell Publishing Ltd, Freshwater Biology, 53, 952–963
 Phytoplankton equilibrium phases 957
nitrification. The re-establishment of thermal stratifica-

(22.4–105.0)

(95.2–190.4)
(23.9–24.7)
(37.0–41.0)

(79.1–89.9)
(449–3249)
(49.0–88.2)

(1.14–1.82)
(28.8–73.2)
(3.3–10.3)
(6.3–7.4)
(7.1–7.8)

(1.0–2.9)
(1.6–4.3)
tion in autumn resulted in a decrease in SRSi concen-

(12–13)
trations but no marked changes in the other nutrients.
VI

24.5
38.9

83.7
1603
70.1
77.9

1.58
49.2
6.9
7.6

2.1
3.0

12

6.8
149.5
Phytoplankton dynamics
Seasonal composition of phytoplankton allowed six

(172.2–215.6)

(226.8 281.4)
different periods to be distinguished (Fig. 5). Three
(19.9–21.2)
(37.0–38.0)

(79.1–89.9)
(944–2724)
(50.4–63.0)

(0.72–1.48)
(26.4–75.6)
(16.8–43.9)
(5.8–6.8)
(7.9–8.7)

(2.0–2.9)
(2.5–6.2)
steady state phases were identified, with different

(5–25)
Table 1 Mean and ranges of limnological variables and compositional features of phytoplankton, in the epilimnion of Faxinal Reservoir in 2004

V (SS)

dominant algal groups: period I was dominated by

Anabaena crassa (Lemmermann) Komárková-Legne-
20.7
37.5

85.9
2173
58.0

1.06
41.7
26.4
6.4
8.4

2.3
4.4

14
192.8

253.1
rová; period III by Nephrocytium sp. and period V by
Asterionella Formosa Hass. Table 1 shows the main
limnological variables of Faxinal Reservoir and the
diversity-related compositional characteristics of its
(26.6–1113.0)

(65.8–1215.2)
(1101–9542)

(21.0–387.8)
(13.7–21.6)
(27.0–55.0)

(30.1–86.1)

(0.02–2.43)

(0.5–357.4)

phytoplankton recorded in the epilimnion during the

(9.0–76.7)
(1 .9–9.6)
(6.5–8.0)
(3.4–8.8)

(0.3–6.7)

(10–25)

six periods.
IV

16.7
38.0

67.4
4133
249.2
219.9

460.8

46.7
25.8
7.2
7.1

2.4
4.8

15
1.23

Period I (January 8–February 10) This period was

characterized by a 6-week long steady state with
dominance of A. crassa making up to 90–99% of total
biomass (Fig. 5). Strong stratification prevailed and
2190 (2078–2423)

87.6 (15.4–219.8)

126.2 (40.6–264.6)

the euphotic zone extended to the entire mixing zone

23.5 (23.1–24.1)

79.9 (78.3–81.3)

38.6 (23.8–53.2)

12.8 (11.5–14.3)

0.71 (0.48–1.05)
51.3 (42.9–63.7)
66.6 (16.9–92.1)
7.4 (7.0–7.6)
7.4 (7.2–7.6)

1.7 (0.8–2.2)

(Fig. 4). The lowest DIN and the highest SRP concen-
20 (13–24)
III (SS)

trations were registered in this period. The highest

stable phytoplankton biomass values (mean value =
27.0

48.3 mg L)1) were found in this period, and species

richness was low (Table 1, Fig. 6).
(1122–2833)
(44.8–221.2)

(40.6–264.6)
(23.8–25.1)
(26.0–27.0)

(78.3–81.3)

(13.0–61.1)

(1.10–2.08)

Period II (February 17–April 6) In late summer an

(7.0–78.4)

(6.2–66.3)
(5.6–39.7)
(7.5–7.9)
(7.2–7.6)

(2.0–6.7)

abrupt shift in phytoplankton composition took place.

(5–24)
II

Cyanobacteria were replaced by several chlorophyte

24.5
26.6

72.5
2223

48.8

25.4

15
1.67
33.2
18.0
7.7
6.6

4.0
119.7

173.7

species without clear dominance patterns (Fig. 5).

This period lasted for 5 weeks during which the
number of taxa and diversity were high (Fig. 6) and
no significant differences in nutrient concentrations
(101.8–111.6)
(1112–4920)

(15.4–201.6)

(89.6–294.0)
(25.0–26.2)
(26.0–28.0)

(53.2–93.8)

(2.8–111.0)

(0.07–0.69)

(11.8–73.9)

occurred compared to period I.

(3.9–12.3)
(7.8–8.0)
(9.1–9.9)

(1.5–2.9)
I (SS)

(5–8)

Period III (April 14–May 5) A second steady state

25.7
27.0

2463
75.1
84.7

39.9

0.28

48.3
7.9
9.4

2.2

6.1
105.5

164.4

phase was identified in autumn in parallel with the

erosion of the thermocline. The colonial green alga
Nephrocytium sp. dominated the assemblage, making
up to 66–90% of total phytoplankton biomass
Conductivity (lS cm)1)

SS, steady state phase.

Diversity (bits mg)1)

(Fig. 5). Phytoplankton diversity was consistently

Richness (no. taxa)

Biomass (mg L)1)

Temperature (C)

low; however, species richness was somewhat

N-N03) (lg L)1)
N-N02) (lg L)1)
N-NH4+(lg L)1)
SRSi (lg L)1)

DIN (lg L)1)

DO (mg L)1)

higher than in the previous period (Fig. 6). Inor-

SRP (lg L)1)

Eveness (%)

ganic nutrient concentrations changed inversely:

% DO

SRP decreased and DIN significantly increased

PH

(Table 1).
 2008 The Authors, Journal compilation  2008 Blackwell Publishing Ltd, Freshwater Biology, 53, 952–963
958 V. Becker et al.
100%
ss ss ss
80%

Biomass
60%

40%

20%

0%
1 3 5 7 9 11 13 15 17 19 21 23 25 27 29 31 33 35 37 39 41 43 45 47 49 51 53 55 Weeks

I II III IV V VI

Asterionella formosa Thalassiosira sp. Anabaena crassa Nephrocytium sp. Others

Fig. 5 Seasonal variation of dominant phytoplankton species biomass (%) in Faxinal Reservoir in 2004. SS, steady state phase.

Richness
no spp. Bits.mg–1
30 Shannon's diversity 3.0
ss ss ss
25 2.5
20 2.0
15 1.5
10 1.0
5 0.5
0 0.0
1 3 5 7 9 11 13 15 17 19 21 23 25 27 29 31 33 35 37 39 41 43 45 47 49 51 53 55 Weeks
I II III IV V VI

Fig. 6 Seasonal variation of species richness (grey bars) and Shannon‘s diversity (black line) in Faxinal Reservoir, in 2004. SS, steady
state phase.

Period IV (June–August 2004) Mixing occurred in this The identified steady-state species were signifi-
period. Phytoplankton biomass was low without cantly correlated with most of the expected environ-
evident dominants but with highly variable diversity mental factors, such as mixing regime, light and
(Figs 5 & 6). High concentrations of DIN and SRSi nutrients (Table 2). A strong correlation was seen
were recorded (Table 1). between A. crassa biomass and temperature
(P < 0.001). This species was also positively correlated
Period V (November 3–December 15) After the onset of with turbidity, water stability and SRP (all P < 0.05),
thermal stratification, high amounts of SRSi allowed and negatively correlated with NO3-N (P < 0.05). In
growth of diatoms. First Thalassiosira sp. started addition, significant positive correlations were
growing but it was rapidly replaced by a fast growing observed between Nephrocytium sp. biomass and both
population of A. formosa. The latter dominated the euphotic and mixing zones; conversely negative rela-
phytoplankton assemblage for more than 2 weeks tionships were found with turbidity and NO3-N (all
(Fig. 5) and this period can be taken as a third P < 0.001). Asterionella formosa biomass was signifi-
equilibrium phase with low diversity values (Fig. 6) cantly positively correlated with NO3-N (P < 0.05),
and decreasing SRSi and DIN (especially nitrate) and negatively correlated with SRSi, SRP (both
concentrations (Table 1). P < 0.001) and NH4-N (P < 0.05).

Period VI (December 15–January 26) After the decline of

Discussion
A. formosa, Thalassiosira sp. started growing again
(Fig. 5). Due to the small size of this diatom, phyto- Dating, at least, back to Hutchinson’s (1961) famous
plankton biomass was low (average = 6.8 mg L)1). paradox, equilibrium and non-equilibrium concepts
SRP dropped below the detection level and might have been a focus of ecological research, both terres-
have been limiting phytoplankton growth as well as trial (see for example Wilson, 1994) and aquatic
SRSi (Table 1). (Padisák, 1994). In fact, contemporary ecology
 2008 The Authors, Journal compilation  2008 Blackwell Publishing Ltd, Freshwater Biology, 53, 952–963
 Phytoplankton equilibrium phases 959
Table 2 Results from Spearman’s correlation between dominant been linked to physical and chemical features of
species biomass and environmental variables (only significant waterbodies the mechanistic explanation comprises:
values P < 0.05 are shown)
(i) water column stability and algal buoyancy control
Biomass (Reynolds, 2006); (ii) high water temperature (Shapiro,
Abiotic
1990); (iii) nutrient content, particularly low N : P
Anabaena Asterionella
variable crassa Nephrocytium sp. formosa ratios (Smith, 1983), high P (Trimbee & Prepas, 1987;
Watson, Mc Cauley & Downing, 1997), (iv) low
Temperature 0.44*
CO2 ⁄ high pH (Shapiro, 1990); (v) low underwater
zeu 0.54*
zmix 0.47* light (Smith, 1986; Havens et al., 1998). Cyanobacterial
Turbidity )0.45* steady states are always accompanied by low diver-
pH 0.37 sity and have been described in many eutrophic lakes
Conductivity )0.28
in the North temperate zones (Elliott, Reynolds &
NH4-N )0.28
NO3-N )0.63 )0.48* 0.40 Irish, 2000; Mischke & Nixdorf, 2003; Morabito et al.,
SRSi )0.35* 2003). These cyanobacterial steady states have been
SRP 0.68 )0.53* attributed to strong vertical segregation of the water
RWCS 0.50
column and the consequent increased selectivity set
SRSi, soluble reactive silicon; SRP, soluble reactive phosphorus; by a reduced mixing depth.
RWCS, relative water column stability. During the autumn, the water column was still
*P < 0.001. stratified, but the RWCS was declining. The mixed
epilimnion and low availability of nutrients contrib-
(whether terrestrial or aquatic) relies heavily on these uted to dominance by Nephrocytium sp., forming the
concepts, either directly or indirectly. It is not unusual second steady state in Faxinal Reservoir. The stronger
in such thoroughly discussed topics for different positive correlations with zeu and zmix, and negative
researchers to have contrasting opinions. Thus, Har- correlations with turbidity and nitrate support this
ris’s (1986) early concepts were principally based on hypothesis. Non-motile Chlorococcales embedded in
physiological ecology of phytoplankton and on mucilage are able to grow under thermal stratification
dynamic features of population changes in lakes. and in a relatively deep optical depth; they are
Here, however, we base our discussion on the more dependent on water turbulence in the epilimnion for
community-ecology oriented concepts originating in resuspension (Happey-Wood, 1988). Green algal
Sommer’s (1983, 1984, 1985, 1989, 1991a,b), and their steady states occur less frequently as compared to
later expansion to temporal changes of phytoplantkon cyanobacteria. There are few described cases from
in natural environments. deeply stratifying water bodies; the filamentous
According to the criteria set by Sommer et al. Planctonema lauterbornii Schmidle was observed in a
(1993), our study has demonstrated the alternation reservoir in France (Leitão et al., 2003) and other
of steady and non-steady state phases of phyto- filamentous green algae may also form a steady state
plankton assemblages dominated by different spe- as indicated, for example, by the recurrent dominance
cies. Each steady state in Faxinal Reservoir of Mougeotia sp. in Lake Garda, Italy (Salmaso &
developed under stratified conditions of the water Padisák, 2007). In two North American lakes, Botryo-
column. The major forces driving the development coccus braunii Kützing has been reported twice in an
and persistence of these steady-state phases seem to equilibrium phase formed by three species (Huszar,
have been closely related to thermal stratification Kruk & Caraco, 2003) of which in one case the
and its consequences. co-dominants were chlorococcalean green algae
The overwhelming dominance of A. crassa, during [Willea wilhelmii (Fott) Komárek and Eutetramorus
summer, constituted the clearest and most obvious planctonicus (Korsikov) Bourrelly]. Nephrocytium sp.,
steady state phase, strongly related to water column which formed the second steady state in Faxinal
stratification parameters, RWCS and temperature. Reservoir, is morphologically similar to Eutetramorus
Low nitrogen concentrations and high SRP favours since both are chlorococcalean, colonial green algal
the growth of this nitrogen-fixing cyanobacterium. species and their colonies are embedded in thick
The dominance of bloom-forming cyanobacteria has mucilage. Clear epilimnia might contribute to the
 2008 The Authors, Journal compilation  2008 Blackwell Publishing Ltd, Freshwater Biology, 53, 952–963
960 V. Becker et al.
success of these species since colonial green algae nutrient availability, size and morphometry, Faxinal
generally have a substantially higher light demand Reservoir does not differ from other reservoirs where
than most planktonic cyanobacteria or diatoms steady state phases have already been recorded (Albay
(Padisák, 2003). & Akcaalan, 2003; Leitão et al., 2003). However, some
After the winter overturn, with low biomass values remarkable features can be emphasized. The first is
and no clear species dominance, the stability of the linked to a longer duration of stratification as com-
water column again started increasing. The more pared to most of the lakes where steady states have
stable conditions in dominance, the water column been previously investigated; the longer period may
stability again started increasing. This more stable allow the establishment of more than one such phase.
environmental condition, in spring favoured the A second reason concerns the geochemical features of
development of the third steady-state (period V), Faxinal Reservoir. It was built on an old geological
due to the rapid increase of the diatom A. formosa. formation with low release of ions and this is
This species has already been observed in steady state combined with high precipitation. These limnological
in lakes and reservoirs of different trophic status peculiarities result in very low conductivity values,
(Albay & Akcaalan, 2003; Morabito et al., 2003). In and consequently in low buffering capacity. The latter,
Faxinal Reservoir, the dominance of this species was along with the anoxic hypolimnetic conditions, allows
significantly correlated with the decrease of dissolved nutrient concentrations to vary over a wide range.
nutrients. The dominance of A. formosa might be However, these changes are not rapid or frequent
related to its fast growth rates coupled to the fact that enough to be classified as disturbance events that
the diatoms are good competitors for nutrients, would prevent the establishment of equilibrium
especially phosphorus (Sommer, 1988). The deficiency phases.
in SRP in this period was probably caused by its
unavailability in the epilimnion due to stratification
Acknowledgments
and little redistribution of nutrients through mixing
(Miller et al., 2005). The observed fluctuations in The authors thank the CT-Hidro ⁄ CNPq (Conselho
A. formosa dominance are probably due to the occur- Nacional de Desenvolvimento Cientı́fico e Tecnológ-
rence of a calm period when most of the population ico), CAPES (Coordenadoria de Aperfeiçoamento de
might have sunk to the bottom of the mixed layer, so Pessoal Superior), Programa de Pós-Graduação em
that its contribution to total biomass was under- Ciências Biológicas (Botânica) – Museu Nacional ⁄
estimated due to the depth of sampling. The sinking UFRJ, and SAMAE (Serviço Autônomo Municipal de
may be halted when cells reach the thermocline, Água e Esgoto de Caxias do Sul) for financial support.
where they may accumulate in the metalimnetic layer Dr Luciane O. Crossetti greatly assisted this work
and eventually be resuspended after a wind event by discussions. We also thank chemical engineer
(Willén, 1991). Fernanda B. Spiandorello and the technicians Graziela
Phytoplankton assemblages are sensitive to peri- P. Monçani and Renivo Girardi, from SAMAE for
odic, largely weather-driven disturbances that prevent their technical support.
succession from proceeding towards an ecological
equilibrium (Reynolds, Padisák & Sommer, 1993). This
References
is the major reason why equilibrium phases rarely
establish in standing waters. Most previous case Albay M. & Akcaalan R. (2003) Factors determining the
studies have reported either a lack of such phases or phytoplankton steady state assemblages in a drinking-
the establishment of only one in a seasonal cycle water Reservoir (Ömerli Reservoir, Istanbul).
(Naselli-Flores et al., 2003). These singular equilibria Hydrobiologia, 502, 85–95.
Allende L. & Izaguirre I. (2003) The role of physical
typically establish either under stressed conditions or
stability on the establishment of steady state in the
in late summer (Padisák et al., 2006; Hajnal & Padisák,
phytoplankton community of two Maritime Antarctic
2008). In this sense, as far as we know, Faxinal
lakes. Hydrobiologia, 502, 211–224.
Reservoir represents a unique case with three phyto- Aminot A. & Chaussepied M. (1983) Manuel des analyses
plankton steady states, involving different major chimiques en milieu marin. CNEXO, Brest.
taxonomic groups during 1 year of study. In terms of
 2008 The Authors, Journal compilation  2008 Blackwell Publishing Ltd, Freshwater Biology, 53, 952–963
 Phytoplankton equilibrium phases 961
Cole G.A. (1994) Textbook of Limnology. Waveland Press Leitão M., Morata S., Rodriguez S. & Vergon J.P. (2003)
Inc, Illinois. The effect of perturbations on phytoplankton assem-
Connell J.H. (1978) Diversity in tropical rainforests and blages in a deep reservoir (Vouglans, France). Hydro-
coral reefs. Science, 199, 1302–1310. biologia 502, 73–83.
Dokulil M. & Teubner K. (2003) Steady state phyto- Lund J.W.G., Kipling C. & Lecren E.D. (1958) The
plankton assemblages during thermal stratification in inverted microscope method of estimating algal num-
deep alpine lakes. Do they occur? Hydrobiologia, 502, ber and the statistical basis of estimating by counting.
65–72. Hydrobiologia, 11, 143–170.
Edler L. (1979) Recommendations for Marine Biological Studies Miller H., Jones I., Folkard A. & Maberly S. (2005) The
in the Baltic Sea; Phytoplankton and Chlorophyll. Unesco, vertical distribution of soluble reactive phosphorus in
Working Group 9, Baltic Marine Biologists, National the water column of Esthwaite water and the effect of
Swedish Environmental Protection Board, Stockholm. physical variables. In: Proceedings of the 9th Workshop on
Elliott J.A., Reynolds C.S. & Irish A.E. (2000) The Physical Processes in Natural Waters (Eds. A. Folkard &
diversity and succession of phytoplankton communi- J. Jones), pp. 183–190. Lancaster University, Lancaster,
ties in disturbance-free environments, using the model, U.K.
PROTECH. Archiv für Hidrobiologie, 149, 241–258. Mischke U. & Nixdorf B. (2003) Equilibrium phase
Ganf G.G. (1974) Diurnal mixing and vertical distribution conditions in shallow German lakes: how cyanobacte-
of phytoplankton in a shallow equatorial lake (Lake ria species establish a steady state in late summer.
George, Uganda). Journal of Ecology, 62, 611–629. Hydrobiologia, 502, 123–132.
Hajnal É. & Padisák J.(2008) Analysis of long-term Morabito G., Oggioni A. & Panzani P. (2003) Phyto-
ecological status of Lake Balaton based on the plankton assemblage at equilibrium in large and deep
ALMOBAL phytoplankton database. Hydrobiologia. subalpine lakes: a case study from Lago Maggiore (N
(in press). Italy). Hydrobiologia, 502, 37–48.
Happey-Wood C.M.(1988) Ecology of freshwater plank- Mullin J.B. & Riley J.P. (1955) The colorimetric determi-
tonic green algae. In: Growth and Reproductive Strategies nation of silicate with reference to sea and natural
of Freshwater Phytoplankton (Ed. C.D. Sandgren), pp. waters. Analytica Chimica Acta, 12, 162–176.
175–226. Cambridge University Press, Cambridge. Murphy J. & Riley J.P. (1962) A modified single-solution
Harris G.P. (1986) Phytoplankton Ecology. Structure, func- method for the determination of phosphate in natural
tion and fluctuation. Chapman and Hall, London. waters. Analytica Chimica Acta, 27, 31.
Havens K.E., Phlips E.J., Cichra M.F. & Li B.L. (1998) Naselli-Flores L., Padisák J., Dokulil M.T. & Chorus I.
Light availability as a possible regulator of cyanobac- (2003) Equilibrium ⁄ steady-state concept in phyto-
teria species composition in a shallow subtropical lake. plankton ecology. Hydrobiologia, 502, 395–403.
Freshwater Biology, 39, 547–556. Padisák J. (1994) Identification of relevant time-scales in
Hillebrand H., Dürselen C-D., Kirschtel D., Pollingher U. non-equilibrium community dynamics: conclusions
& Zohary T. (1999) Biovolume calculation for pelagic from phytoplankton surveys. New Zealand Journal of
and benthic microalgae. Journal of Phycology, 35, 403–424. Ecology, 18, 169–176.
Honti M., Istvanovics V. & Osztoics A. (2007) Stability Padisák J. (2003) Phytoplankton. In: The Lakes Handbook 1.
and change of phytoplankton communities in a highly Limnology and Limnetic Ecology (Eds P.E. O’Sullivan &
dynamic environment – the case of large shallow Lake C.S. Reynolds), pp. 251–308. Blackwell Science Ltd.,
Balaton (Hungary). Hydrobiologia, 581, 225–240. Oxford.
Huszar V., Kruk C. & Caraco N. (2003) Steady-state Padisák J., Reynolds C.S. & Sommer U. (1993) Intermediate
assemblages of phytoplankton in four temperate lakes Disturbance Hypothesis in Phytoplankton Ecology. Devel-
(NE, USA). Hydrobiologia, 502, 97–109. opments in Hydrobiology ⁄ Hydrobiologia 249, Kluwer
Hutchinson G.E. (1961) The paradox of plankton. The Acad. Publ. Dordrecht, Boston, London, pp 199.
American Naturalist, 95, 37–147. Padisák J., Borics G., Fehér G., Grigorszky I., Oldal I.,
Jensen P., Jeppesen E., Olrik K. & Kristensen P. (1994) Schmidt A. & Zámbóné-Doma Z. (2003a) Dominant
Impact of nutrients and physical factors on the shift species, functional assemblages and frequency of
from cyanobacterial to chlorophyte dominance in equilibrium phases in late summer phytoplankton
shallow Danish lakes. Canadian Journal of Fisheries and assemblages in Hungarian small shallow lakes.
Aquatic Sciences, 51, 1692–1699. Hydrobiologia, 502, 157–168.
Köppen W. (1936) Das geographische System der Klimate - Padisák J., Barbosa F., Koschel R. & Krienitz L. (2003b)
Handbuch der Klimatologie, Vol. 1, Part C, Gebr. Born- Deep layer cyanoprokaryota maxima are constitutional
träger Verlag, Berlin. features of lakes: examples from temperate and

 2008 The Authors, Journal compilation  2008 Blackwell Publishing Ltd, Freshwater Biology, 53, 952–963
962 V. Becker et al.
tropical regions. Archiv für Hydrobiologie, Special Issues, Sommer U. (1985) Comparison between steady-state and
Advances in Limnology, 58, 175–199. non steady-state competition: experiments with natu-
Padisák J., Borics G., Grigorszky I. & Soróczki-Pintér É. ral phytoplankton. Limnology and Oceanography, 30,
(2006) Use of phytoplankton assemblages for monitor- 335–346.
ing ecological status of lakes within the Water Frame- Sommer U. (1988) Growth and survival strategies of
work Directive: the assemblage index. Hydrobiologia, planktonic diatoms. In: Growth and Reproductive Strat-
553, 1–14. egies of Freshwater Phytoplankton (Ed. C.D. Sandgren),
Pielou E.C. (1966) The measurement of diversity in pp. 227–260. Cambridge University Press, Cambridge.
different types of biological collections. Journal of Sommer U. (1989) The role of competition for resources
Theoretical Biology, 13, 131–144. in phytoplankton succession. In: Plankton Ecology:
Reynolds C.S. (2006) The Ecology of Phytoplankton (Ecol- Succession is Plankton Communities. (Ed. U. Sommer),
ogy, Biodiversity and Conservation). Cambridge Univer- pp. 57–106. Springer, Berlin.
sity Press, Cambridge. Sommer U. (1991a) The application of Droop-model of
Reynolds C.S., Padisák J. & Sommer U. (1993) Interme- nutrient limitation to natural phytoplankton. Verhandl-
diate disturbance in the ecology of phytoplankton and ungen der internationale Vereinigung für theoretische und
the maintenance of species diversity: a synthesis. angewandte Limologie, 24, 791–794.
Hydrobiologia, 249, 183–188. Sommer U. (1991b) A comparison of the Droop-model
Rojo C. & Álvarez-Cobelas M. (2003) Are the steady state and the Monod.model of nutrient limitated growth
phytoplankton assemblages in the field? Hydrobiologia, applied to natural populations of phytoplantkon.
502, 3–12. Functional Ecology, 5, 535–544.
Rott E. (2002) Is the persistence of the Cylindrospermopsis Sommer U., Padisák J., Reynolds C.S. & Juhász-Nagy P.
raciborskii and Fragilaria acus dominated phytoplankton (1993) Hutchinson‘s heritage: the diversity-disturbance
in a shallow tropical reservoir indicating equilibrium relationship in phytoplankton. Hydrobiologia, 249, 1–7.
conditions? In: Abstracts of the 13th Workshop IAP (Ed. Sommer U., Sommer F., Santer B., Zöllner E., Jürgens K.,
L. Naselli-Flores), pp. 49. Castelbuono, Italy, 31 Jamieson C., Boersma M. & Gocke K. (2003) Daphmia
August-8 September, 2002. versus copepod impact on summer phytoplankton:
Salmaso N. & Padisák J. (2007) Morpho-Functional functional compensation at both trophic levels. Oeco-
Groups and phytoplankton development in two deep logia, 135, 639–647.
lakes (Lake Garda, Italy and Lake Stechlin, Germany). Strickland J.D.H. & Parsons T.R. (1972) A Practical
Hydrobiologia, 578, 97–112. Handbook of Seawater Analysis. Fisheries research board
Shannon C.E. & Weaver W. (1949) The Mathematical of Canada. Bulletin 167. 2nd edn. Ottawa.
Theory of Communication. Univ Illinois Press, Urbana. Tilman D. (1977) Resource competition between plank-
Shapiro J. (1990) Currents beliefs regarding dominance tonic algae: an experimental and theoretical approach.
by blue-greens: the case of the importance of CO2 and Ecology, 58, 338–348.
pH. Verhandlungen der Internationalen Vereinigung für Trimbee A.M. & Prepas E.E. (1987) Evaluation of total
Theoretische und Angewandte Limnologie, 24, 38–54. phosphorus as a predictor of the relative biomass of
Smith V. (1983) Low nitrogen to phosphorous rations blue-green algae with emphasis on Alberta lakes.
favor dominance by blue-green algae in lake phyto- Canadian Journal of Fisheries and Aquatic Sciences, 44,
plankton. Science, 221, 669–671. 1337–1342.
Smith V. (1986) Light and nutrient effects on the relative Uhelinger V. (1964) Étude statistique des méthodes de
biomass of blue-green algae in lake phytoplankton. dénobrement planctonique. Archive Science, 17, 121–123.
Canadian Journal of Fisheries and Aquatic Sciences, 43, Utermöhl H. (1958) Zur vervollkommung der quantita-
148–153. tiven phytoplankton - methodik. Mitteilungen der
Solorzano L. (1969) Determination of ammonia in natural internationale Vereinigung für Theoretische und Ange-
waters by phenol hypochlorite method. Limnology and wandte Limnologie, 9, 1–38.
Oceanography, 14, 799–801. Watson S.B., Mc Cauley E. & Downing J.A. (1997)
Sommer U. (1983) Nutrient competition between Patterns in phytoplankton taxonomic composition
phytoplankton in multispecies chemostat experiments. across temperate lakes of differing nutrient status.
Archiv für hydrobiologie, 96, 399–416. Limnology and Oceanography 42, 487–495.
Sommer U. (1984) The paradox of plankton: fluctuations Wetzel R.G. & Likens G.E.(2000) Limnological Analyses.
of phosphorus availability maintain diversity in flow- 3rd edn. Springer-Verlag New York Inc, New York.
through cultures. Limnology and Oceanography, 29, Whittaker R.H. (1975) Communities and Ecosystems.
633–636. Macmillan, New York.

 2008 The Authors, Journal compilation  2008 Blackwell Publishing Ltd, Freshwater Biology, 53, 952–963
 Phytoplankton equilibrium phases 963
Willén E. (1991) Planktonic diatoms – an ecological Wood E.D., Armstrong F.A.J. & Richards F.A. (1967)
review. Algological Studies, 62, 69–106. Determination of nitrate in sea water by cadmium-
Wilson J.B. (1994) The intermediate disturbance copper reduction to nitrite. Journal of the Marine
hypothesis of species coexistence is based on patch Biological Association, 47, 23–31.
dynamics. New Zealand Journal of Ecology, 18, 176–
181. (Manuscript accepted 11 December 2007)

 2008 The Authors, Journal compilation  2008 Blackwell Publishing Ltd, Freshwater Biology, 53, 952–963