Aquat Ecol (2009) 43:285–293 DOI 10.1007/s10452-008-9164-0
Diel variation of phytoplankton functional groups in a subtropical reservoir in southern Brazil during an autumnal stratification period Vanessa Becker Æ Luciana de Souza Cardoso Æ Vera Lu´cia M. Huszar
Received: 14 May 2007 / Accepted: 2 January 2008 / Published online: 22 January 2008 Ó Springer Science+Business Media B.V. 2008
Abstract A knowledge of diel variation and the vertical distribution of phytoplankton communities may contribute to a better understanding of the driving factors of key species. Applying functionalgroup classification provides important information on the causes of species selection in the pelagic community. The diel variation of phytoplankton functional groups was analysed during an autumnal stratification period with the aim of understanding their changes in the vertical position related to light, mixing regime and grazing pressure. Phytoplankton and zooplankton communities were sampled every 4 h during a 24-h period in a vertical profile in a subtropical meso-eutrophic reservoir. Strong stratification during a 24-h cycle and a mixed clear epilimnion with partial atelomixis marked the autumn season in the Faxinal reservoir, southern Brazil. The highest phytoplankton densities and biomass were found during the second part of the day, a general pattern reported in the literature, and may be
V. Becker (&) V. L. M. Huszar Laborato´rio de Ficologia, Museu Nacional do Rio de Janeiro, Universidade Federal do Rio de Janeiro, Quinta da Boa Vista s/n°, Sa˜o Cristova˜o, Rio de Janeiro 20940-040, Brazil e-mail:
[email protected] L. de Souza Cardoso Instituto de Biocieˆncias, Dept. Botaˆnica, Universidade Federal do Rio Grande do Sul, Av., Bento Gonc¸alves 9500, Porto Alegre 91501-970, Brazil
explained by zooplankton dynamics. During the 24-h cycle, phytoplankton functional groups lacking a self-regulating capacity and those able to regulate their vertical position were vertically segregated in the lake. The diel behaviour of both groups was driven by the mixing regime (including atelomixis), light and zooplankton grazing pressure. Keywords Atelomixis Grazing Man-made lake Phytoplankton dynamics Stratification 24-hour cycle
Introduction A knowledge of diel and vertical distribution of phytoplankton communities may contribute to a better understanding of the factors regulating key species. Such a dynamics has been well documented for both temperate (Maulood et al. 1978; Frempong 1981; Takamura and Yasuno 1984) and tropical and subtropical ecosystems (Barbosa and Padisa´k 2002; Melo et al. 2004; Lopes et al. 2005). In general, the cited studies are based on the density or biomass of major taxonomical groups, and most related diel and vertical phytoplankton distribution to: (1) mixing properties, including atelomixis (diurnal mixing restricted to the epilimnion); (2) occurrence of selfregulating populations by flagella or aerotopes; (3) occurrence of fast-growing species, which can
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change in abundance during a single diel cycle. Herbivorous zooplankton may also regulate these phytoplankton populations (DeMott 1989; Reynolds 2006). Diel vertical migration of large zooplankton is a common phenomenon in the pelagic zone of lakes. These zooplankters can move through the water column twice a day, migrating downward into the darker water layers during the day and upward into surface levels at night (Gliwicz and Pijanowska 1988; Reichwaldt and Stibor 2005). Phytoplankton species have developed morphological and physiological adaptive strategies for surviving in different environments (Reynolds 1998), including adaptations to particular diel and vertical dynamics. Based on Grime’s (1979) seminal work on terrestrial vegetation and using morphological and physiological traits, Reynolds (1997) defined several phytoplankton functional groups that potentially, and alternatively, may dominate or co-dominate in a given environment (Reynolds et al. 2002). These are often polyphyletic and share adaptive features, based on the physiological, morphological and ecological attributes of the species. Nowadays, the phytoplankton functional groups approach comprises 31 assemblages that are identified by alphanumerical codes according to their sensitivities and tolerances (Reynolds 2006). This phytoplankton functional groups approach applied to aquatic systems provides important information for understanding the dynamic of species selection in the pelagic communities in temperate (Huszar et al. 2003; Leita˜o et al. 2003), tropical (Lopes et al. 2005; Sarmento et al. 2007) and subtropical regions (Fabbro and Duivenvorden 2000; Kruk et al. 2002). The study reported here was carried out in a subtropical, warm monomictic, meso-eutrophic reservoir in South Brazil during well-stratified conditions, low epilimnetic nutrient concentrations and a relatively clear epilimnion (unpublished data). We analysed the diel variation of phytoplankton functional groups during an autumnal stratification period with the aim of gaining an understanding of their changes in vertical position as related to light, mixing regime and grazing pressure. Earlier studies have reported that phytoplankton population densities increase during the second part of the day (Frempong 1981; Melo et al. 2004), although a consistent explanation for this has not yet appeared in the literature. Consequently, we hypothesized that total
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phytoplankton densities and biomass would increase during the early afternoon. We also hypothesized that phytoplankton functional groups without self-regulating capacity (which will be distributed according to the segregated layers) and those able to regulate their vertical position in the water column will be driven by a mixing regime and light and by zooplankton grazing pressure. This hypothesis is based on the autecology’s phytoplankton functional groups related to their adaptations to the environmental changes (Reynolds 2006).
Study site Faxinal reservoir (29°050 0000 S; 51°030 3000 W) is the main water supply source for the city of Caxias do Sul (population 400,000) in southern Brazil (Fig. 1). The sampling station is located near the water intake, in the deepest part of the reservoir. It is 3.1 km2 in area and situated at an altitude of 700 m a.s.l. The reservoir is deep (zmax = 30 m) and is a mesoeutrophic system [annual means in the epilimnion: total phosphorus (TP) 0.92 lM; chlorophyll a 15 lg l-1; Becker, unpublished data]. Faxinal is a warm monomictic reservoir (winter overturn), with a metalimnion localized between 5 and 8 m and a well-marked thermal gradient. A large
Fig. 1 Map of Faxinal reservoir, showing the tributaries and the sampling station (P1)
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hypolimnion layer is anoxic during 7 months of the year (Becker et al. 2008). The reservoir is located in a subtropical region with a temperate regional climate, without a dry season (Cfa; Ko¨ppen 1936). The annual mean temperature is 16°C, and the total annual precipitation ranges between 1800 and 2200 mm. During this study, the Faxinal reservoir was thermally stratified, with a clear mixed epilimnion, low nutrient levels (mean values dissolved inorganic nitrogen (DIN) 7.31 lM; soluble reactive phosphorus (SRP) 0.14 lM] and slightly alkaline conditions. Some environmental variables, mainly nutrients, were segregated in the water column (Becker et al. unpublished data) (Table 1).
Methods Sampling and field measurements Samples were collected near the water intake (sampling station), in the deepest part of the reservoir (zmax = 30 m), every 4 h during a 24-h period in the autumn of 2004 (May 11–12) along a vertical profile (surface, 3, 10 and 30 m) with a Van Dorn bottle (2 l). The autumn was selected because during this season the reservoir is stratified, which is the representative of most (80%) of the whole year. One sample was collected at each depth. The criteria for sampling were based on the sampling protocol of the Water Company in 2002: weekly algal Table 1 The main water chemistry parameters of the Faxinal Reservoir during the study period (May 2004) (measured only in the first shift)
All values are given as the mean followed by the maximum–minimum values (in parenthesis) SRSi, Soluble reactive silicate; SRP, soluble reactive phosphorus; DIN, dissolved inorganic nitrogen; TN, total nitrogen; TP, total phosphorus
monitoring (at the surface) and monthly nutrient analyses in the water sampling station of the Faxinal Reservoir (Becker et al. 2008). Four sampling stations have been studied, and no significant differences were found among these for any of the variables studied (Becker et al. unpublished data). P1 was chosen in this study due to its importance for the monitoring of the water intake. Depths were defined as a function of light (surface and 3 m), zooplankton pressure grazing (10 m) and the sinking process (30 m) based on the monitoring data. Temperature, dissolved oxygen (DO), pH and conductivity were measured with a Horiba (model U-10) probe each 1-m depth. Transparency was estimated with a Secchi disk and turbidity with a HACH 2100P turbidimeter. Phytoplankton was sampled with a Van Dorn bottle (2 l) and fixed with neutral Lugol´s solution. Zooplankton was sampled integrating the upper 10-m layer using a suction pump and plankton net (25-lm mesh size) and fixed with formaldehyde (4%).
Sample analysis Phytoplankton populations were enumerated in random fields (Uhelinger 1964) using the settling technique (Utermo¨hl 1958). The units were enumerated to at least 100 specimens of the most frequent species (Lund et al. 1958). Zooplankton was counted in a Sedgwick-Rafter chamber (APHA 1992). A minimum of 100 individuals were counted for the
Water chemistry parameters
Epilimnion
Hypolimnion
Free CO2 (mg l-1)
7 (6–8)
36 (31–40)
N-NH+4 (lM) N-NO2 (lM) N-NO3 (lM)
5.31 (2.4–8.2)
32.21 (10.2–54.2)
0.04 (0.02–0.06)
0.08 (0.05–0.11)
1.96 (1.7–2.2)
0.42 (0.42)
SRSi (lM)
212.8 (116.2–309.3)
285.2 (277.7–92.7)
SRP (lM)
0.14 (0.13–0.15)
0.46 (0.2–0.73)
DIN (lM)
7.31 (4.7–9.9)
32.71 (10.6–54.8)
TN (lM)
222.0 (202.3–241.7)
290.5 (260.5–320.5)
TP (lM)
0.97 (0.65–1.29)
5.49 (2.58–8.4)
TN/TP (by atom)
265 (157–374)
78 (31–124)
DIN/SRP (by atom)
53 (37–68)
64 (54–75)
SRSi/SRP (by atom)
1519 (922–2115)
906 (400–1412)
Chlorophyll a (lg l-1)
9.64 (6.14–13.14)
1.61 (0.21–3.0)
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zooplankton, with a minimum of 80% efficiency (Pappas and Stoermer 1996).
Data analysis The euphotic zone (zeu) was calculated as three times the Secchi disk extinction depth (Cole 1994). The mixing zone (zmix) was defined by the thermal and DO vertical gradients. Algal biovolume was calculated using formulae for geometric shapes (Hillebrand et al. 1999) and assuming the fresh weight unit as expressed in mass, where 1 mm3 l-1 = 1 mg l-1 (Wetzel and Likens 2000). Species contributing [5% to the total biomass were grouped into functional groups using the criteria of Reynolds et al. (2002). The size fractions of phytoplankton (0–10, 11–20, 21–30, [30 lm) were defined according to the size of food selected by herbivorous zooplankton reported in literature (Reynolds 2006). These fractions were estimated based on algal GALD (greatest axial linear dimension) (Lewis 1976). The functional groups of zooplankton were defined according to food size and feeding habits: small filter-feeders up to 200 lm GALD (herbivorous protists [ 25 lm and rotifers), medium filter-feeders up to 1 mm GALD (cladocerans and copepod nauplii), carnivores (copepod Cyclopoida) and detritivorous (protists [ 25 lm). Zooplankton biomass (fresh weight) was calculated using formulae for geometric shapes (Dumont et al. 1975; Bottrell et al. 1976; Ruttner-Kolisko 1977; Malley et al. 1989). A two-way ANOVA test (STATISTICA ver. 5.0; SPSS, Chicago, IL) was used to compare the means of the phytoplankton biomass and density among depthtime (hours) variation.
Results Light, mixing regime and water chemistry Air temperature, measured in each sampling time, showed the highest values between 10:00 and 14:00 hours (16.5–18.2°C, respectively) and the lowest at 02:00 hours. (10.7°C). A thermal stratification, with clear mixed epilimnion extending to about the upper 8 m was observed. A 5-m euphotic zone (zeu) extended between 58 and 81% of the mixing
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zone. The hypolimnion layer (23 m) was in complete anoxia and extended from a depth of 7 m to the reservoir bottom (Fig. 2). During the night and early morning, it was possible to recognize a partial mixing of the epilimnion (atelomixis) (Fig. 2). A marked vertical stratification of DO concentrations throughout the study was observed. The surface water layer was sub-saturated in DO during the 24-h cycle, with the highest concentrations (72%) in the afternoon (14:00 hours). Strong stratification and layer segregation were also shown by the high values of turbidity, conductivity, iron and manganese in the hypolimnion (Table 2).
Plankton communities A total of 56 algal species were distributed in seven major taxonomic categories, with most summarized in six functional groups. The F and H groups were the most important in terms of biomass and were represented by colonial green algae with thick mucilaginous sheaths (Nephrocytium sp. and Eutetramorus fottii) and N-fixing cyanobacterium (Anabaena crassa), respectively. Also important in terms of biomass were the green algae Coelastrum reticulatum (J), the euglenoids Trachelomonas bacillifera, T. volvocina and T. volvocinopsis (W2) and the diatoms Aulacoseira granulata (P) and Thalassiosira sp. (A). By pooling the entire dataset, significant differences in total phytoplankton biomass (F = 10.6; df = 3; P \ 0.001) and density (F = 4.7; df = 3; P \ 0.01) among depths were found but not in time. However, if we consider depths separately, significant differences were not found only between 10 and 30 m. This is why phytoplankton biomass results were analysed only in the upper 10-m layer. Two general patterns of phytoplankton densities and biomass were found: (1) higher values in the epilimnion (0–8 m), mainly during the two illuminated periods; (2) lower values in the epilimnion during the beginning of the night (Fig. 3). This biomass behaviour was mainly represented by changes in non-motile colonial green algae (F and J), N-fixing cyanobacteria (H) and small centric diatoms (A) (Fig. 4). Heavy microplanktonic diatoms (P) and euglenoids (W2) increased in the hypolimnion in different periods of the 24-h cycle (Fig. 4). Group
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Fig. 2 Profiles of water temperature and dissolved oxygen (DO) during the 24-h cycle in Faxinal reservoir
W2 occurred mainly in the afternoon, whereas group P increased from the non-illuminated to the illuminated period (Fig. 4). Phytoplankton size data were integrated in the upper 10 m layer in order to relate them to zooplankton biomass. The dominant phytoplankton fraction was between 21 and 30 lm. The main representative in this spectrum size was the green algae (Oocystaceae, Chlorococcales) Nephrocytium sp. (group F), which contributed [60% to this size
Table 2 Abiotic variables in the epi- and hypolimnion of Faxinal reservoir during a 24-hour cycle All values (with the exception of Secchi transparency) are given as the mean followed by the maximum–minimum values (in parenthesis)
class. Other size fractions of phytoplankton (1–10 lm and 11–20 lm) contributed only 0.4 and 9.5%, respectively (Fig. 5). Thus, the predominant phytoplankton size class in this study was in the edible size range (21–30 lm) for cladocerans. Zooplankton biomass in the upper 10 m layer was higher in the middle of the first morning (10:00 hours) and at the beginning of the non-illuminated period (18:00 hours), showing a increased gradient up to 02:00 hours. The increase of zooplankton at the
Abiotic variables
Epilimnion
Hypolimnion
Secchi transparency (m)
1.59
–
Water temperature (°C)
18.2 (17.7–19.5)
14.2 (13.7–14.9)
pH
7.8 (7.1–8.1)
7.7 (7.3–8.8)
Conductivity (lS cm-1)
28 (28)
92 (60–212)
Dissolved oxygen (%)
59.1 (49.7–67.8)
0.2 (0–0.6)
Turbidity (NTU)
4.9 (3–10)
12.1 (1–101)
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Fig. 3 Depth-time diagrams (upper 10 m of the water column) of phytoplankton: biomass (mg l-1) (a) and density (ind ml-1) (b) during a 24-hour cycle in Faxinal reservoir
Fig. 4 Depth-time diagrams (upper 10 m) of F, H, J, A, W2 and P functional group biomass (mg l-1) during a 24-hour cycle in Faxinal reservoir
beginning of the night suggests an upward vertical migration (Fig. 5). The dominant zooplankton functional group was the medium filter feeders, mainly
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represented by Cladocera (Daphnia ambigua, D. gessneri, Ceriodaphnia cornuta, Bosmina hagmanni and B. longirostris).
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Fig. 5 Phytoplankton integrated biomass of the size classes (a) and biomass of zooplankton functional groups (b) in the epilimnion of Faxinal reservoir during a 24-h cycle
Discussion Stratification, buoyancy, capacity for vertical regulation, light regime and grazing can potentially control phytoplankton biomass and species composition (e.g. Smith and Bennet 1999). In Faxinal reservoir, stratified conditions were observed during the 24-h study period, with a clear epilimnion and conspicuous water column segregation. In addition, many species with the ability to migrate, either by using their flagella or aerotopes, were present. Non-motile species with thick mucilaginous sheaths were important contributors to the total biomass and also formed vertically segregated populations in the water column. Because phytoplankton functional groups are better related to environmental variability than individual species or major taxonomical groups, we used this approach to analyse the diel variation in Faxinal reservoir. The main phytoplankton functional groups (F, H, A) increased in biomass during the day and decreased at night in the epilimnion. The dominant functional group, F, was represented by non-motile colonial green-algae enveloped by mucilaginous sheaths (Nephrocytium sp., Eutetramorus fottii); these are usually reported as being adapted to
clear, little-enriched, stratified systems (Reynolds et al. 2002). Unexpectedly, a diatom (Thalassiosira sp., group A) maintained itself in the stratified epilimnion during the illuminated periods. The resistance to sinking was improved by this diatom’s small size (diameter 13 lm) and, consequently, by its high surface area-to-volume ratio (Padisa´k et al. 2003a). The partial atelomixis also favoured the maintenance of non-motile groups F and A, playing a key role in keeping these suspended in the epilimnion (Barbosa and Padisa´k 2002). During the day, when a strong stratification occurred, the self-regulating group, H (Anabaena crassa), was also important in the epilimnion. Indeed, water-column stability is an important condition for cyanobacteria development, mainly for species with aerotopes, such as Anabaena, which are positively buoyant plankters (Reynolds 2006). Another vertical and diel pattern emerged in the hypolimnion during the afternoon and early morning. The anoxic hypolimnion, with high organic matter content, may favour the ‘bottom-dweller’ flagellates that are adapted to mixotrophic conditions and able to migrate in the vertical column (group W2, Trachelomonas spp.). This functional group and group P (Aulacoseira granulata), formed by a heavy
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filamentous diatom, increased in this layer. This last group may be interpreted as a deposit of the ’ecological memory’ of the community, here considered as the capacity of past states to influence present or future responses (Padisa´k 1992). Diatoms as memory species have been reported for other stratified lakes (Padisa´k et al. 2003b). Top-down control also may act upon the phytoplankton biomass dynamic during a 24-h cycle. An inverse pattern of the zooplankton biomass in relation to phytoplankton was observed during the night in Faxinal reservoir. Grazing pressure has been found to be important at this time, mainly in tropical lakes with efficient filter feeders such as Daphnia spp. and Bosmina spp. (Perticarrari et al. 2003). Zooplankton grazing rates can be about fivefold higher during the evening than during other periods of the day (Crumpton and Wetzel 1982). Zooplankton have been found to spend the night in the warmer, foodrich upper layers (epilimnion) and migrated downward into the darker, lower layers (hypolimnion) during the day (Reichwaldt and Stibor 2005). Daphnia can tolerate temporary anoxia for refuge in the hypolimnion anoxic, despite the reduction in the growth rate and reproductive effort (Dawidowicz et al. 2002). The dominant Nephrocytium sp. (group F) was the main edible species because it is within the appropriate size spectrum (21–30 lm, with the mucilaginous sheath) to be grazed by the cladocerans (Cyr and Curtis 1999; Reynolds 2006). The zooplankton grazing pressure at night, due to their vertical migration, may be a plausible explanation for the general pattern of higher phytoplankton populations during the second part of the day previously reported by several authors and summarized by Melo et al. (2004). In summary, our study confirmed that the distribution of phytoplankton functional groups in a 24-h cycle was clearly related to the environmental conditions. Strong stratification and a clear epilimnion with partial atelomixis marked the autumn season in the Faxinal reservoir. The highest phytoplankton densities and biomass was found during the second part of the day, a general pattern reported in literature. This pattern can be explained by zooplankton dynamics. During the 24-h cycle, phytoplankton functional groups without self-regulating capacity and those able to regulate their vertical position were
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differentially distributed in the segregated layers. The diel behaviour of both groups was driven by the mixing regime (including atelomixis), light and zooplankton grazing pressure. Acknowledgements The authors thank the CT-Hidro/CNPq (Conselho Nacional de Desenvolvimento Cientı´fico e Tecnolo´gico), CAPES (Coordenadoria de Aperfeic¸oamento de Pessoal Superior), Programa de Po´s-Graduac¸a˜o em Cieˆncias Biolo´gicas (Botaˆnica)—Museu Nacional/UFRJ, and SAMAE ´ gua e Esgoto de Caxias do (Servic¸o Autoˆnomo Municipal de A Sul). We are grateful to Dr. Judit Padisa´k for her kind revision and valuable comments on the manuscript. We also thank chemical engineer Fernanda B. Spiandorello; Graziela P. Monc¸ani and Renivo Girardi, technicians from SAMAE, for technical support; and finally Haywood Dail Laughinghouse IV and Janet W. Reid for revising the English text.
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