Spatial and temporal dynamics of phytoplankton functional group in a
blocked valley (Brazil).
N A B O U T1 , 2, J . C . & N O G U E I R A1, I . S . 1 D e p a r t a m e n t o d e B i o l o g i a , L a b o r a t ó r i o d e L i m n o l o g i a , I C B 1 , U n i v e r s i d a d e F e d e r a l d e G o i á s ,
C . P. 1 3 1 , C a m p u s I I – G o i â n i a - G O , B r a s i l . C E P. 7 4 0 0 1 - 9 7 0 . e - m a i l : n o g u e i r a @ i c b . u f g . br
2 P r o g r a m a d e D o u t o r a d o e m C i ê n c i a s A m b i e n t a i s , U n i v e r s i d a d e F e d e r a l d e G o i á s , C . P. 1 3 1 , C a m p u s I I – G o i â n i a - G O , B r a s i l . C E P. 7 4 0 0 1 - 9 7 0 . e - m a i l : n a b o u t j c @ h o t m a i l . c o m
ABSTRACT: Spatial and temporal dynamics of phytoplankton functional group in a blocked valley (Brazil). L a k e T i g r e s i s a b l o c k e d - v a l l e y l a k e , f o r m e d b y t r i b u t a r y o b s t r u c t i o n f r o m s e d i m e n t d e p o s i t i o n d u r i n g f l o o d i n g i n t h e m a i n c o u r s e o f t h e r i v e r . F e w s t u d i e s h a v e t r e a t e d phytoplankton dynamics in blocked-valley lakes. The aim of this study was to investigate the temporal and spatial patterns of phytoplankton biovolume, to detect and describe the dominant phytoplankton functional groups in Lake Tigres during the dry season and the b e g i n n i n g o f t h e r a i n y s e a s o n i n 2 0 0 4 . T h e m e a n p h y t o p l a n k t o n b i o v o l u m e w a s <0.4mm3.L- 1, characterizing Lake Tigres as oligotrophic. During the entire study period, 18
functional groups were found, with a predominance of phytoflagellate functional groups (Y, W1, W2, Lo) and some diatoms (N, P, D). Because of limnological differences in each sampling period, the functional groups were different in each month and principally between the dry and rainy seasons, which was shown by canonical correspondence analysis (CCA). The CCA indicated that in the dry season, the predominant functional groups Y, W1, W2, and Lo were favored by higher nutrient concentrations and high oxygen content. At the beginning of the rainy season, the predominant functional groups P, S1, S, T and N were favored by surface drainage and high water temperature. The dry-season biovolume samples were characterized by nanoplankton species (C-strategists), suggesting that small size is an optimal strategy for nutrient absorption. However, during the early rainy season, biovolume was dominated by microplankton species (SR-strategists).
Key words: Lake Tigres, dry and rainy seasons, tropical environment.
RESUMO: Dinâmica espacial e temporal de grupos funcionais fitoplanctônicos de um vale bloqueado (Brasil). O lago dos Tigres pode ser caracterizado como um vale bloqueado, formado atra-vés da obstrução de tributários e pela deposição de sedimentos durante a inundação a partir do curso principal. Poucos trabalhos abordaram a dinâmica fitoplanctônica em vales bloqueados, para tanto, o objetivo desse trabalho foi reconhecer os padrões de distribui-ção temporal e espacial do biovolume fitoplanctônico e detectar os grupos funcionais fitoplanctônicos dominantes e descritivos do sistema lago dos Tigres durante o período de seca (junho a setembro) e início de chuva (outubro e novembro) de 2004. Os valores de b i o v o l u m e f i t o p l a n c t ô n i c o , e m m é d i a , f o r a m i n f e r i o r e s a 0 , 4 m m3.L- 1, c a r a c t e r i z a n d o o
sistema lago dos Tigres como oligotrófico. Durante todo período de estudo foram encon-t r a d o s 1 8 g r u p o s f u n c i o n a i s , s e n d o q u e o p r e d o m í n i o f o i d e g r u p o s f u n c i o n a i s d e fitoflagelados (Y, W1, W2 e Lo) e de algumas diatomáceas (N, P e D). Devido às diferenças limnológicas em cada período de amostragem os grupos funcionais foram relativamente diferentes em cada mês e principalmente entre os períodos de seca e chuva, o que ficou evidenciado pelos escores derivados da análise de correspondência canônica (ACC). A ACC indicou ainda que, na estiagem os grupos funcionais Y, W1, W2 e Lo foram beneficia-dos pela maior concentração de nutrientes e elevada saturação de oxigênio, enquanto que durante o período de elevada precipitação os grupos funcionais predominantes foram P, S1, S, T e N, favorecidos pelo escoamento superficial e elevada temperatura da água. Na s e c a o b i o v o l u m e d o s p e r í o d o s d e a m o s t r a g e m f o i c a r a c t e r i z a d o p o r e s p é c i e s nanoplanctônicas, (C-estrategistas), sugerindo que no sistema Lago dos Tigres o pequeno t a m a n h o s e j a u m a e s t r a t é g i a p a r a o t i m i z a r a a b s o r ç ã o d o s n u t r i e n t e s . P o r o u t r o l a d o durante o período de elevada precipitação o biovolume foi caracterizado por espécies microplanctônicas (SR-estrategistas).
Introduction
Taxonomic groups of phytoplankton are c o m p o s e d o f s p e c i e s w i t h v e r y d i f f e r e n t p h y s i o l o g i e s , s o t h e a n a l y s i s o f phytoplankton functional groups can better reveal the physiological, morphological, and ecological responses of the phytoplankton c o m m u n i t y t o e n v i r o n m e n t a l c o n d i t i o n s ( R e y n o l d s , 2 0 0 6 ) . F u n c t i o n a l g r o u p s o f phytoplankton are polyphyletic groups that r e s p o n d s i m i l a r l y t o a d e t e r m i n e d s e t o f environmental conditions (Reynolds et al., 2 0 0 2 ; R e y n o l d s , 2 0 0 6 ) . T h e i r a n a l y s i s p r o v i d e s a b e t t e r u n d e r s t a n d i n g o f phytoplankton dynamics than describing the dynamics of taxonomic groups (Kruk et al., 2 0 0 2 ; R e y n o l d s e t a l . , 2 0 0 2 ; R e y n o l d s , 2 0 0 6 ) . P r e s e n t l y , 3 1 p h y t o p l a n k t o n functional groups are described (Reynolds et al., 2002). I n i t i a l l y t h e f u n c t i o n a l g r o u p s w e r e s t u d i e d i n t e m p e r a t e e n v i r o n m e n t s ; h o w e v e r , t h i s c o n c e p t a p p e a r s t o b e a p p r o p r i a t e f o r t r o p i c a l e n v i r o n m e n t s a s w e l l . C u r r e n t l y , p h y t o p l a n k t o n f u n c t i o n a l groups are receiving much attention, and h a v e e n h a n c e d d e s c r i p t i o n s o f t h e dynamics of the community of taxonomic groups (Reynolds, 1997; Kruk et al., 2002; Reynolds et al., 2002; Nabout et al., 2006). Analysis of functional groups has been shown to be appropriate for tropical regions. H o w e v e r , n o s t u d i e s h a v e f o c u s e d o n phytoplankton functional groups in blocked-valley lakes. This type of lake is formed by s e d i m e n t d e p o s i t i o n o b s t r u c t i n g t h e tributary during flooding of the main course (Kalff, 2002). This characteristic of Lake Ti-gres results in different dynamics from other fluvial lake types. An important difference b e t w e e n b l o c k e d - v a l l e y a n d o t h e r f l u v i a l lakes (oxbow, meander scroll, and others) i s t h e i r h y d r o l o g i c a l c o n n e c t i v i t y. T h i s connectivity has a great impact on dynamics a n d b i o d i v e r s i t y , b e c a u s e i t a f f e c t s t h e exchange of energy and matter (organisms) between the river and its floodplain (Bini et al., 2003).
T h e s t u d y o f s p a t i a l a n d t e m p o r a l variability is fundamental to understand the structure and function of the phytoplankton c o m m u n i t y a n d a l s o t o u n d e r s t a n d t h e d y n a m i c s o f a q u a t i c e c o s y s t e m s . Phytoplankton fluctuations can be predictive and make it possible to recognize changes
in the aquatic environment (Huszar, 2000). The aim of this study was to recognize the t e m p o r a l a n d s p a t i a l p a t t e r n s o f phytoplankton distribution, and detect the d o m i n a n t a n d d e s c r i p t i v e p h y t o p l a n k t o n f u n c t i o n a l g r o u p s i n t h i s b l o c k e d v a l l e y (Lake Tigres system) during the dry season and the beginning of the rainy season of 2004. We attempted to answer the following questions: (i) Was there any temporal change i n f u n c t i o n a l g r o u p s , m a i n l y b e t w e e n t h e dry season and the beginning of the rainy season? (ii) Was there any spatial change i n p h y t o p l a n k t o n f u n c t i o n a l g r o u p s , predominantly between the lotic and lentic regions of the Lake Tigres system? (iii) Which limnological variables were associated with t h e s e s p a t i a l a n d t e m p o r a l c h a n g e s i n phytoplankton functional groups? (iv) Do the phytoplankton functional groups provide a g o o d d e s c r i p t i o n o f t h e l i m n o l o g i c a l characteristics of the Lake Tigre system?
Material and methods
The source of the Lake Tigres system is the Água Limpa River. It is located in the Britânia district of western Goiás state, cen-tral Brazil, in the Tocantins-Araguaia basin, a t r i b u t a r y o f t h e Vermelho River ( Fig. 1 ) . Lake Tigres is large, 24.5 km long with a 60.83 km perimeter, and is a popular tourist d e s t i n a t i o n .
There were 11 sampling stations, three in lotic regions (Água Limpa and the Ver-m e l h o R i v e r ) a n d e i g h t i n l e n t i c r e g i o n s ( L a k e T i g r e s ) , n e a r p r e s e r v e d a n d d e f o r e s t e d a r e a s a n d a p o p u l a r t o u r i s t r e g i o n .
S a m p l e s w e r e c o l l e c t e d i n t h e d r y season (June, July, August, and September) a n d t h e b e g i n n i n g o f t h e r a i n y s e a s o n ( O c t o b e r a n d N o v e m b e r ) o f 2 0 0 4 . Subsurface 100 mL samples were collected for quantitative study; they were placed in dark bottles, fixed with lugol-acetic solution (Vollenweider, 1974), and stored in the dark. T h e d e n s i t y o f t h e p h y t o p l a n k t o n w a s e s t i m a t e d b y t h e U t e r m ö h l m e t h o d ( U t e r m ö h l , 1 9 5 8 ) , w i t h a L e i t z i n v e r t e d microscope, at a magnification of 450x. The individuals (cells, colonies, cenobios, and filaments) were counted in random fields; about 100 individuals of the most frequent species were counted, with less than 20% error, at a confidence limit of 95% (Lund et al., 1958).
A l g a e b i o v o l u m e w a s a p p r o x i m a t e d a c c o r d i n g t o H i l l e b r a n d e t a l . ( 1 9 9 9 ) a n d e x p r e s s e d i n m m3.L- 1. P h y t o p l a n k t o n
f u n c t i o n a l g r o u p s w e r e d e t e r m i n e d f r o m species that represented more than 5% of the biovolume of at least one sample unit ( K r u k e t a l . , 2 0 0 2 ) . T h e p h y t o p l a n k t o n functional groups were defined according to Reynolds (1997) and Reynolds et al. (2002). L i m n o l o g i c a l c h a r a c t e r i z a t i o n o f t h e lake was based on chemical and physical water information, measured at the same d e p t h a s t h e p h y t o p l a n k t o n s a m p l i n g a t each collection station. Variables measured were: water temperature, pH, conductivity, total dissolved solids, and oxygen saturation using a HORIBA U-21 water multianalyzer. W a t e r t r a n s p a r e n c y a n d d e p t h w e r e m e a s u r e d b y S e c c h i d i s c . T h e e u p h o t i c zone was calculated as 3 times the depth of Secchi disc disappearance (Cole, 1994).
Water samples were also collected from each site for total nitrogen and phosphorus analysis. They were fixed in the field with 0 . 5 m L a b s o l u t e s u l f u r i c a c i d . C o l l e c t i o n procedures and laboratory processing were a d o p t e d f r o m M a c k e r e t h e t a l . ( 1 9 7 8 ) , Carmouze (1994), and Clesceri et al. (1992).
Floristic dissimilarity between months was measured by the Bray-Curtis index. The functional group data and matrix were used to form the dendrogram, using Bray-Curtis d i s s i m i l a r i t y a n d t h e U P G M A c o n n e c t i o n m e t h o d ( S n e a t h & S o k a l , 1 9 7 3 ) . T h e cophenetic coefficient of correlation (r) was c a l c u l a t e d t o e v a l u a t e m a t r i x a n d dendrogram dissimilarity.
R e l a t i o n s h i p s b e t w e e n a b i o t i c a n d biovolume data were evaluated by canonical correspondence analysis (CCA; Ter Braak, 1 9 8 6 ) . T h e n u l l h y p o t h e s i s o f a b s e n c e o f r e l a t i o n s h i p b e t w e e n m a t r i c e s ( b i o t i c a n d a b i o t i c ) w a s t e s t e d w i t h M o n t e C a r l o procedures. The lines of environmental data matrixes were randomly allocated and the CCA was calculated. The entire procedure was repeated 1000 times. Species of algae a n d e n v i r o n m e n t a l d a t a w e r e p r e v i o u s l y transformed (Log(n+1)). All calculations were done with the PC-ORD program (McCune & Mefford, 1997).
Results
La k e T i g r e s i s a b l o c k e d - v a l l e y l a k e , s h a l l o w a n d w i t h l o w t r a n s p a r e n c y. The l i m n o l o g i c a l v a r i a b l e s s h o w e d s p a t i a l
Figure 1: Location of area study, indicating the sampling station
BRITÂNIA
Lake
Tigres
2.500 0 2.500 5000m 51° 1 7’ 00’’ 51° 1 7’ 00’’ 51° 06 ’ 00’’ 51 ° 06’ 00’’ 15° 10’ 0 0” 15° 1 0 ’ 0 0 ” 15° 21’ 00’’ 0 1 5° 21’ 0 ’’ Arco-Iris Stream Luanda Stream 0 4250 Km 1 2 3 4 5 6 7 8 9 10 11 Vermelho river Tigrinho lake Boa S orte Stream Á gua Fr i as tre am Eld or a do St re am Ág ua Li m pa riv er Scale 1:250.000 Ve rm e lho riverTable I: Limnological variables measures registered at the lake Tigres. The mean and standard deviation (SD) are calculated for six samplings in Lake Tigres.
Limnological variables
June
July August September October November
SD 1.23 1.06 0.99 1.02 1.21 1.10 Depth Mean (m) 3.93 3.02 2.75 2.24 2.21 2.70 SD 0.13 0.10 0.16 0.06 0.07 0.07 Transparency Mean (m) 0.49 0.52 0.51 0.40 0.45 0.32 SD 0.38 0.31 0.49 0.19 0.22 0.20 Euphotic Zone Mean (m) 1.46 1.57 1.52 1.21 1.34 0.96 SD 0.88 0.70 2.05 1.84 1.38 2.23 Water temp. Mean (°C) 25.32 25.94 26.19 28.17 30.45 32.01 SD 14.08 7.51 5.84 9.21 13.74 8.86 Conductivity Mean (µS.cm-1) 46.25 31.82 22.62 28.64 46.21 30.91 SD 6.20 6.86 7.98 29.12 9.93 12.19 Ox. Saturation Mean (%) 100.88 111.00 131.64 168.91 134.54 155.82 SD 0.46 0.66 0.25 0.40 0.61 0.28 pH Mean 7.30 7.51 6.95 6.81 7.61 7.20 SD 99.86 69.97 68.76 68.68 35.08 54.25 Total Nitrogen Mean (µg.L-1) 230 148.18 94.55 68.18 81.36 139.89 SD 46.60 57.68 76.66 48.79 53.73 25.19 Total phosphorus Mean (µg.L-1) 52.50 52.27 58.18 50.00 37.73 29.95 (between lotic and lentic regions) and
tem-poral differences (between the dry season and the beginning of the rainy season) (Tab. I). In the dry season, the samples revealed higher nutrient concentrations (June, July, and August) and oxygen saturation (September).
At the beginning of the rainy season (November), water temperatures were higher (Nabout & Nogueira, given in publication). These temporal variations demonstrated the strong influence of the hydrological cycle on limnological variables.
The phytoplankton biovolume showed different horizontal patterns in the lake over six sampling periods, mainly between the dry season and the beginning of the rainy season. During all sampling periods, algae biovolume was low (Fig. 2), from 0.035
mm3.L-1 (Station 1 - November) to 1.64 mm3.L- 1
( S t a t i o n 4 - S e p t e m b e r ) . To t a l b i o v o l u m e t e n d e d t o w a r d s h i g h e r v a l u e s f r o m September onward.
D u r i n g t h e s t u d y p e r i o d , m e a n
biovolume values were less than 0.4 mm3.L-1.
T h e r e f o r e , L a k e T i g r e s i s a n o l i g o t r o p h i c e n v i r o n m e n t , u s i n g R e y n o l d s ( 1 9 8 4 ) b i o v o l u m e v a l u e s f o r t r o p h i c s t a t e characterization. The highest phytoplankton biovolume values were recorded at Station 4 in September (F i g. 2D; Euglena sp.) and Station 10 in November (Fig. 2F; Aulacoseira granulata var. angustissima).
Because of limnological differences in each sampling period, the functional groups w e r e r e l a t i v e l y h e t e r o g e n e o u s i n e a c h month. Species that contributed at least 5% o f t h e t o t a l b i o v o l u m e a t e a c h s a m p l i n g station were represented by 18 functional g r o u p s o v e r t h e e n t i r e s t u d y p e r i o d . However, there was a general predominance of phytoflagellate functional groups (Y, W1, W 2 , a n d L o ) w i t h s o m e d i a t o m s a n d desmids (N, P, and D) (Fig. 3).
D u r i n g J u n e , g r o u p s P a n d D w e r e dominant in the lotic region (stations 1, 10, and 11), whereas phytoflagellates (functional groups Y, W2, and Lo) were dominant at all other (lentic) sampling stations.
In July and August, functional group Y w a s a b u n d a n t a t a l m o s t a l l L a k e T i g r e s s a m p l i n g s t a t i o n s . A l s o i n t h e s e m o n t h s C y c l o t e l l a s p . 1 ( f u n c t i o n a l g r o u p A ) w a s
Figure 2: Biovolume of the phytoplankton community (mm3.l- 1) o f t h e l a k e T i g r e s i n a l w a y s m o n t h s o f s a m p l i n g s t a t i o n . T h e l e t t e r s a b o v e t h e b a r i n d i c a t e t h e r e p r e s e n t a t i v e f u n c t i o n a l g r o u p s , according to Reynolds et al. (2002).
Figure 3: Relative contribution (%) of representative phytoplankton functional groups of Lake Tigres in sampling period of 2004.
a b u n d a n t a t S t a t i o n 1 1 ( l o t i c r e g i o n ) , comprising 23% and 79% of this station’s
t o t a l b i o v o l u m e i n J u l y a n d A u g u s t , respectively.
D u r i n g S e p t e m b e r a t S t a t i o n 1 , functional group D (Cocconeis placentula ) had a total biovolume of 35%. Stations 10 and 11 were abundant in Cyclotella sp.1 with 5 3 % a n d 6 2 % o f t h e t o t a l b i o v o l u m e r e s p e c t i v e l y . F l a g e l l a t e s w e r e a l w a y s p r e s e n t , w i t h h i g h b i o v o l u m e s a t m o s t s t a t i o n s , w i t h S t a t i o n 4 h a v i n g g r o u p W 1 (Euglena sp.) as dominant with 83% of the total biovolume.
I n O c t o b e r a n d N o v e m b e r i n t h e beginning of the rainy season, a change in dominant functional groups was observed. I n O c t o b e r t h e f u n c t i o n a l g r o u p S 1 h a d e l e v a t e d b i o v o l u m e s , b e i n g d o m i n a n t a t S t a t i o n s 1 , 7 , a n d 8 w i t h 2 5 % , 5 4 % , a n d 5 7 % o f t h e t o t a l b i o v o l u m e , r e s p e c t i v e l y. I n N o v e m b e r, f u n c t i o n a l g r o u p N (Haplotaenium minutum ) w a s d o m i n a n t a t S t a t i o n s 7 a n d 9 . I n t h e s a m e m o n t h , functional group P ( Aulacoseira granulata var. angustissima) was dominant in the lotic region (Stations 10 and 11), with 75% and 48% of the total biovolume, respectively.
D i s s i m i l a r i t y a n a l y s i s b a s e d o n p h y t o p l a n k t o n f u n c t i o n a l g r o u p d a t a ( F i g . 4 ) s h o w e d t h a t t h e p h y t o p l a n k t o n community was formed by similar functional groups in the months of July and August.
Functional groups Y and Lo predominated in these two months (F i g. 3). October and N o v e m b e r w e r e d i s t i n g u i s h e d f r o m t h e other months by the presence of functional groups N, P, and Lo. September showed a m o r e d i s t i n c t p h y t o p l a n k t o n c o m m u n i t y t h a n o t h e r m o n t h s , p r o b a b l y b e c a u s e o f elevated biovolumes and a predominance of functional group W1.
The first two axes of the canonical correlation analysis (CCA – Fig. 5) explained only 20.5% (12.1% axis 1; 8.3% axis 2) of total data variability. The Monte Carlo Test (Table II) indicated that the first three canonical correlations were significant (p<0.05).
E n v i r o n m e n t a l v a r i a b l e s p o s i t i v e l y c o r r e l a t e d w i t h t h e f i r s t a x i s w e r e transparency, total phosphorus, and oxygen s a t u r a t i o n ; w h e r e a s t h o s e n e g a t i v e l y c o r r e l a t i n g w i t h t h e s e c o n d a x i s w e r e o x y g e n s a t u r a t i o n a n d e l e c t r i c a l c o n d u c t i v i t y . C C A o r d i n a t i o n o f phytoplankton functional groups suggested t h a t g r o u p s Y , W 2 , L o , N , a n d D w e r e correlated with low nutrient concentrations at most stations in June, July, and August. These functional groups (or at least one of them) were always abundant in at least one sampling station.
Figure 4: Dendrogram of the dissimilarity coefficient, when phytoplankton of the lake Tigres was obtained on basis of the functional groups with more than 5 % of the total biovolume of each sampling s t a t i o n . ( r = 0 . 7 8 ) . November October August September July June
Bray Curtis Coeficient
Axes
Species –
environment
Mean
Minimum
Maximum
P
1 0.798 0.615 0.355 0.854 0.012
2 0.662 0.467 0.243 0.710 0.007
3 0.495 0.370 0.179 0.685 0.032
Table II: Statistical data of Monte Carlo test—species–environment correlations for Lake Tigres. Species– e n v i r o n m e n t c o r r e l a t i o n , c a n o n i c a l c o r r e l a t i o n ; M e a n , c a n o n i c a l c o r r e l a t i o n a v e r a g e o b t a i n e d with the aleatory data; Minimum, minimum value of the canonical correlation obtained with the aleatory data; Maximum, maximum value of the canonical correlation obtained with the aleatory data; P, significance level.
F u n c t i o n a l g r o u p Y w a s i m p o r t a n t i n t e r m s o f b i o v o l u m e i n J u n e , J u l y , a n d August (dry season). These small organisms a r e f o u n d i n p r a c t i c a l l y a l l a q u a t i c e n v i r o n m e n t s , p r i n c i p a l l y t r o p i c a l l a k e s . According to Klaveness (1988) and Sommer ( 1 9 8 1 ) , t h e y p r e f e r m i x i n g o f t h e w a t e r column by wind, because they have greater a d a p t a b i l i t y t o t u r b u l e n t w a t e r c o l u m n mixing and low transparency conditions. The i d e a l e n v i r o n m e n t f o r t h i s g r o u p i s moderately nutrient-rich water, because they a r e w e l l a d a p t e d t o l o w l i g h t l e v e l s (Reynolds et al., 2002).
C C A f o r L a k e T i g r e s ( F i g . 5 ) demonstrated that functional group Y was
Discussion
In floodplain lakes, flooding is a factor regulating phytoplankton species biovolume in tropical regions, e.g., in the Paraná River ( T h o m a z e t a l . , 1 9 9 7 ; T r a i n & R o d r i g u e s , 1997), the Amazon floodplain (Melo & Huszar, 2000), and the Pantanal floodplain (Oliveira & C a l h e i r o s , 2 0 0 0 ; J u n k e t a l . 2 0 0 6 ) . H o w e v e r , i n b l o c k e d - v a l l e y l a k e s , t h e climate regime and consequent increase in w a t e r c o l u m n a r e a l s o i m p o r t a n t f a c t o r s . The Lake Tigres system showed changes i n t h e b i o v o l u m e a n d p h y t o p l a n k t o n c o m p o s i t i o n d u r i n g t h e b e g i n n i n g o f t h e rainy season (Fig. 2).
Figure 5: Scores derived from the canonical correspondence analysis (CCA) applied to the biovolume dominant phytoplankton species and environmental variables. The numbers represent the station sampling and the letter the phytoplankton functional groups according Reynolds et al. (2002). Codes for the environmental variables are CND, electrical conductivity; OX, oxygen saturation; TRA, water transparency; TN, total nitrogen and TP, total phosphorous.
correlated with stations that showed higher nutrient contents (phosphorus) and lower t r a n s p a r e n c y . I n f u n c t i o n a l g r o u p Y , C r y p t o m o n a s e r o s a , C . m a r s o n i i, a n d C . obovata were responsible for the highest b i o v o l u m e v a l u e s . T h e s e s p e c i e s w e r e characterized by Olrik (1994) as C-strategists, with high surface/volume ratios, facilitating rapid growth by rapid nutrient absorption. Functional group Y was also abundant in Lake Castelo in the Paraguay River (Olivei-ra & Calheiros, 2000), in lakes of the Upper Paraná River during the dry season (Train & Rodrigues, 2004), and in floodplain lakes of the Middle Araguaia River, mainly during l o w - w a t e r p e r i o d s ( N a b o u t e t a l . 2 0 0 6 ) , where sampling characteristics were simi-l a r t o t h o s e f o u n d i n L a k e T i g r e s d u r i n g June, July, and August. In the Araguaia River l a k e s , a s w e l l a s a p r e d o m i n a n c e o f C r y p t o p h y c e a e , b i o v o l u m e v a l u e s a l s o tended to be oligotrophic, as observed in this study. Lakes Dumbazinho, Landi, and J a p o n ê s ( N a b o u t e t a l . , 2 0 0 6 ) w e r e a l s o classified as blocked valleys by Morais et al. (2005); when information from Lake Ti-gres was compared with these lakes, there w e r e s o m e s i m i l a r i t i e s i n p h y t o p l a n k t o n functional groups, such as dominant group Y i n t h e 2 0 0 0 d r y s e a s o n a n d d o m i n a n t group W1 in Lake Japonês in the 2000 rainy s e a s o n .
P h y t o p l a n k t o n f u n c t i o n a l g r o u p s W 2 ( Tr a c h e l o m o n a s s p . 4 a n d S t r o m b o m o n a s verrucosa ) and Lo (Peridinium umbonatum and P. corillionii) were also abundant in June, J u l y , a n d A u g u s t . A l l t h e s e g r o u p s w e r e c i t e d b y R e y n o l d s e t a l . ( 2 0 0 2 ) a s b e i n g adapted to moderately nutrient-rich waters. I n t h i s s t u d y , t h e C C A d e m o n s t r a t e d t h a t t h e s e f u n c t i o n a l g r o u p s w e r e c o r r e l a t e d w i t h m o r e - c o n c e n t r a t e d n u t r i e n t environments. Functional group Lo was also abundant in the Middle Paraná River (Garcia de Emiliani, 1993). Functional group W2 was also abundant during low-water periods in s o m e A r a g u a i a R i v e r l a k e s ( N a b o u t e t a l . 2 0 0 6 ) . I n J u n e , J u l y , a n d A u g u s t , t h e B a c i l l a r i o p h y c e a e c o m p r i s e d f u n c t i o n a l g r o u p s A ( C y c l o t e l l a s p . 1 ) a n d D ( G o m p h o n e m a p a r v u l u m a n d C o c c o n e i s p l a c e n t u l a ) . F u n c t i o n a l g r o u p s A a n d D (Baccilariophyceae) require turbulence and l o w l i g h t l e v e l s , a n d h a v e a t e n d e n c y t o grow in eutrophic environments (Sommer, 1988). Both functional groups, according to t h e C C A ( F i g. 5 ) , w e r e c o r r e l a t e d w i t h
locations where total nitrogen was higher and water transparency lower than in other areas in Lake Tigres. These species mainly occurred at Stations 1 (Água Limpa River), 1 0 , a n d 1 1 ( b o t h i n t h e Ve r m e l h o R i v e r ) . Because these were lotic region stations, they showed high turbulence and probably high silica availability, since the sediment was sand or clay.
A n a l y s i s o f d i s s i m i l a r i t y ( F i g . 4 ) d e m o n s t r a t e d t h a t t h e b e g i n n i n g o f t h e r a i n y s e a s o n p r o v o k e d d i f f e r e n t i a t i o n i n p h y t o p l a n k t o n f u n c t i o n a l g r o u p composition. Physical and chemical analysis of Lake Tigres water (Nabout & Nogueira, g i v e n i n p u b l i c a t i o n ) i n d i c a t e d h i g h t e m p e r a t u r e s a n d l o w t r a n s p a r e n c y i n October and November. Detailed analysis of phytoplankton functional groups in these months showed a predominance of different phytoflagellate and diatom groups.
D u r i n g O c t o b e r a n d N o v e m b e r , functional groups S and N were abundant at some stations. These groups are to be f o u n d i n t u r b i d a n d m e s o t r o p h i c environments (Reynolds et al., 2002). The class functional group S has been reported a s b e i n g a t h o m e i n e n v i r o n m e n t s w i t h elevated temperatures (Shapiro, 1990) and h i g h t u r b u l e n c e ( G a n f , 1 9 8 3 ) . F u n c t i o n a l group N was reported as being quite well a d a p t e d t o l o w - l i g h t a n d h i g h - t u r b u l e n c e environments (Happey-Wood, 1988). Groups S a n d N a r e S R - s t r a t e g i s t s , w h i c h c a n m i n i m i z e g r a z i n g ( O l r i k , 1 9 9 4 ) , m a i n l y because of their size or cell shape.
Analysis of dissimilarity (Fig. 4) and CCA ( F i g . 5 ) d e m o n s t r a t e d t h a t S e p t e m b e r d i f f e r e d f r o m a l l t h e o t h e r m o n t h s . C C A showed that sampling stations in this month showed correlations between high oxygen s a t u r a t i o n v a l u e s a n d a d o m i n a n c e o f f u n c t i o n a l g r o u p W 1 ( E u g l e n o p h y c e a e ) . I n t h e A r a g u a i a R i v e r f l o o d p l a i n l a k e s , functional group W1 was co-dominant with g r o u p P d u r i n g t h e h i g h - w a t e r p e r i o d (Nabout et al., 2006). According to Reynolds et al. (2002), this functional group can be f o u n d i n s h a l l o w e n v i r o n m e n t s , w i t h v e g e t a t i o n o r o t h e r s o u r c e s o f o r g a n i c matter, and requires high dissolved oxygen c o n t e n t s .
In summary, phytoplankton biovolume r e s p o n d e d t o t h e c l i m a t e r h y t h m , b e i n g different in each period. The dry and early r a i n y s e a s o n s s h o w e d d i f f e r e n t phytoplankton dynamics; CCA highlighted the importance of the hydrological cycle for
phytoplankton dynamics. There was spatial d i f f e r e n t i a t i o n b e t w e e n l o t i c a n d l e n t i c environments. The predominant functional groups at the lotic stations were P, A, and D ; a n d a t t h e l e n t i c s t a t i o n s w e r e Y , W 1 , W 2 , a n d L o . T h e r e f o r e , a n a l y s i s o f t h e phytoplankton functional groups provided a g o o d d e s c r i p t i o n o f t h e L a k e T i g r e s system, better representing the spatial and temporal phytoplankton dynamics and the influence of limnological variables.
Acknowledgements
We are grateful to Secretaria de Ciên-c i a e T e Ciên-c n o l o g i a d o E s t a d o d e G o i á s ( S E C T E C - G O ) f o r f i n a n c i a l s u p p o r t o f t h e project, to the CNPq for their grant of the D T I s c h o l a r s h i p f o r J . C . N . ( P r o c . 5 0 7 2 7 4 / 2004-0), and to the Agência Ambiental de Goiás for analysis of physical-chemical data. We also thank Dra. Vera L. M. Huszar (Mu-seu Nacional/ UFRJ), Dr. Luis M. Bini (Uni-v e r s i d a d e F e d e r a l d e G o i á s ) f o r c r i t i c a l comments on our manuscript, Dr. Edgardo Latrubesse (Universidade Federal de Goiás) f o r g e o m o r p h o l o g i c a l c h a r a c t e r i z a t i o n o f Lake Tigres, Dr. Janet W. Reidfor the revision o f t h e E n g l i s h l a n g u a g e a n d t h e t w o a n o n y m o u s r e f e r e e s w h o m a d e h e l p f u l comments on the manuscript.
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Received: 19 February 2007 Accepted: 19 October 2007
