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Plankton dynamics and photosynthesis responses in a eutrophic lake in Patagonia (Argentina): influence of grazer abundance and UVR/Dinamica del plancton y respuestas fotosinteticas en una laguna eutrofica de Patagonia (Argentina): influencia de la abundancia de herbivoros y RUV.

INTRODUCTION

The seasonal variations of environmental factors often result in changes of phytoplankton species composition, as each species has different requirements and characteristics (Floder et al., 2002). Since growth and production of phytoplankton are closely related to photosynthesis, temperature and solar radiation are two of the key physical variables controlling algal populations in a particular season in highly eutrophic waters (Schoor et al., 2008). For example, it has been recently shown in a mesocosm study that while solar radiation has an important role in the initiation of the spring bloom, an increase in temperature may decrease the peak biomass, mean cell size and the share of diatoms in the phytoplankton community (Sommer & Lengfellner, 2008). The penetration of solar radiation into the water column depends on several factors, but in many cases particulate matter (such as phytoplankton)--POM and dissolved matter (such as chromophoric dissolved organic matter, CDOM) constitute the main attenuators (Morris et al., 1995). Thus, light availability in the water column may have a strong influence in shaping the producers' community. For example in shallow water lakes of Argentina, light limitation contributes to a lower periphyton development as compared to that of phytoplankton (which can be take advantage of surface light while is transported by mixing) whereas in less light-limited waters periphyton may develop a high biomass (Sanchez et al., 2010). Additionally, grazing plays a significant role in shaping the phytoplankton seasonal succession: In some lakes, for example, grazing pressure may reduce a considerable portion of phytoplankton biomass (Sommer et al., 1993; Floder & Sommer, 1999) sometimes inducing a "clear-water" phase (Lampert & Sommer, 1997). In these cases, phytoplankton cells need to cope not only with grazing pressure, but also with enhanced underwater radiation that can be potentially harmful (Williamson et al., 2007).

In regard to solar radiation, a vast literature exists about the negative effects produced by ultraviolet wavelengths (UVR, 280-400 nm) on different cellular targets of plankton organisms: The DNA molecule, proteins and photosynthetic apparatus, among others see review by Hader et al. (2007). In particular, the decrease of photochemical quantum yield, associated with photo inhibition (Osmond, 1994) has been extensively studied in diverse aquatic organisms such as macroalgae, phytoplankton and microphytobenthos (Villafane et al., 2003). While this photo-inhibition is mostly caused by PAR, UVR can also have considerable effects (Sinha et al., 2001a; Klisch et al., 2005). UVR-induced photoinhibition is known to change seasonally depending on the composition of the natural assemblages, as seen in Patagonian marine coastal waters where the bloom (diatom-dominated) was relatively more sensitive that the pre- and post bloom communities (flagellate-dominated community) (Villafane et al., 2004a). In turn, the differential sensitivity of species could lead to changes in the taxonomic composition of the community (Worrest et al., 1981) sometimes in a time-scale of days-weeks (Silva et al., 2008). In sites with strong seasonal variations, such as mid-latitudes, the penetration of solar radiation will also change with time, thus producing a variable underwater radiation field throughout the year, depending on ambient physics, chemistry and biology (Bracchini et al., 2004). Therefore it is relevant to consider all of these variables when experimentally studying the responses of the photosynthetic apparatus due to UVR exposure in different communities occurring throughout the seasonal cycle.

Additionally, a number of studies have investigated the effects of zooplankton feeding when algae cells were exposed to UVR. For example, De Lange et al. (2000) found that when grazers were absent, in situ UVA could stimulate algae growth, with UVB acting in the opposite direction. Daphnia clearance rates, however, showed large variations and were not significantly different in the radiation treatments used in the experiments. Short-term laboratory experiments showed that in general, females of the cladoceran Daphnia magna may ingest higher amounts of algae treated with high doses of artificial UVB (Germ et al., 2004). This could be a way to compensate changes in cells, mediated by a UVB-induced reduction in digestibility (Van Donk & Hessen, 1995). Ultimately, grazers such as Daphnia may be affected by UVR-mediated changes in phytoplankton as a food source (Hessen et al., 1997). This may influence life history traits and fitness of Daphnia, depending on which phytoplankton species are used as a food source (De Lange & Van Reeuwijk, 2003). Additionally, short-term effects in laboratory may be different (and even contradictory) when considering different species of grazers and phytoplankton (De Lange & Lurling, 2003). Overall, most of these studies where performed with laboratory cultures and artificial UVR sources, while much less information is available for natural algae and grazers communities (i.e., which are exposed to strong seasonal changes in solar radiation, among other factors). In a recent paper Williamson et al. (2010) found that UVR did not influence zooplankton grazing in a mountain lake. However, the authors argued that considering the effects of UVR on the reproduction, plankton responses to UVR may be altered by changes in zooplankton population sizes as well as the direct response of phytoplankton to UVR and grazing. These long-term effects, however, were difficult to observe within the time frame of their experiments (i.e., 7 days) (Williamson et al., 2010).

It is clear that direct and indirect long-term effects of UVR on natural phytoplankton and zooplankton communities are difficult to predict. Moreover, studies with integrated observations and experiments on natural phytoplankton communities under solar radiation in a year-round sampling strategy are still scarce. Thus, the objective of this study is to evaluate the in situ seasonal dynamics of phytoplankton throughout the year and its relationships with both grazers and UVR, and how photochemical performance (in terms of photochemical quantum yield measurements) varies with taxonomic composition. Our working hypotheses were that: a) phytoplankton species composition and relative dominance throughout the year is shaped both by grazers and UVR, and b) photochemical performance is related to the taxonomic composition and thus it changes seasonally with phytoplankton community.

MATERIALS AND METHODS

Sampling site

In situ measurements and samplings were carried out at Lake Cacique Chiquichano, which is a eutrophic, shallow (max depth ca. 2 m), small lake/pond (0.18 [km.sup.2]). The lake is located within the city of Trelew, Argentina (43[degrees]14.9'S, 65[degrees]17.9'W, population ca. 80,000 inh) and therefore it is exposed to some anthropogenic influence. Its waters often show a high chlorophyll concentration, in accordance with its high nutrient load throughout the year. The mean concentration of nutrients in the water during summer, autumn, winter and spring were: 30.9, 122.2, 192, and 44.3 [micro]M of nitrogen (N[O.sub.2.sup.-] + N[O.sub.3.sup.-]), 16.5, 8.8, 36.6, and 58.8 [micro]M phosphate (P[O.sub.4.sup.-3]), and 280, 506, 518, and 434 [micro]M silicate (Si[O.sub.4.sup.-2]), respectively (Goncalves, unpublished data). The absence of trees or tall buildings in its surroundings allows the water surface to be exposed to full solar radiation and also to the influence of strong winds that induce mixing in the whole water column. The lake is in a region subjected to a wide range of temperatures, solar radiation and wind intensity during the annual cycle (Helbling et al., 2005). Some studies were previously carried out with natural phytoplankton communities from this lake to evaluate DNA damage caused by ultraviolet B (UVB, 280-315 nm) exposure (Klisch et al., 2005) whereas the main grazers (cladocerans) were studied with respect of their tolerance (survival and motility) to UVR (Goncalves et al., 2002, 2007).

Water samples were collected throughout an annual cycle, from February 2005 to January 2006, with a frequency of once every 2-4 weeks. Sampling was conducted in the afternoon or evening before experimentation. Samples of zoo- and phytoplankton were collected from a fixed station on the shore (considered representative of the whole lake) and placed in 20-L plastic carboys previously cleaned with water and HCl (1 N). Water temperature was recorded in situ and the plankton samples were taken to the laboratory within 40 min. for subsequent determinations and experiments.

Zooplankton

We determined the abundance of copepods and cladocerans throughout the year and this data was used to later infer the grazing pressure of crustacean zooplankton on phytoplankton communities. Zooplankton samples were taken with a plankton net (200 [micro]m) and fixed with formaline (~2% final formaldehyde concentration). The abundance of the cladoceran Daphnia spinulata Biraben, 1917 and the cyclopoid copepod Metacyclops mendocinus (Wierzejski, 1892)--the two species that characterized the zooplankton community throughout the year--were determined by considering the number of individuals (counted under a stereoscope) and the volume of water filtered.

Phytoplankton

Determinations of phytoplankton chlorophyll-a (chl-a) and cell concentration were conducted at the laboratory with traditional methods. Chl-a was determined in vitro for the total and < 20 [micro]m(pico-nanoplankton) fraction after filtering 50-100 mL of sample (using Wathman GF/F filters, 25 mm in diameter) and extracting the pigments in 7 mL of absolute methanol (Holm-Hansen & Riemann, 1978). The chl-a concentration was calculated from the fluorescence readings (before and after acidification with HCl) using a Turner Designs fluorometer (TD700). Pigments absorbance was also measured from these methanol extracts by doing a scan between 250 and 750 nm with an spectrophotometer (Hewlett Packard 8453E). Cell concentration and taxonomic composition was determined on preserved samples (0.4% formaldehyde) using the Uthermol sedimentation method as described by Villafane & Reid (1995) and with an inverted microscope. A drop of Rose Bengal was added to the Uthermol chamber to better distinguish between small organic and inorganic particles. For each sampling date, phytoplankton species richness (S) was recorded as the total number of species present in a given sample. Each different species contributed to S even if it was not fully identified (e.g., Scenedesmus sp.1, Scenedesmus sp. 2, etc.).

Exposure experiments

These experiments were designed to evaluate the effects of solar radiation on photochemical performance of phytoplankton. A 10-L water sample was pre-filtered (200 [micro]m, to remove larger grazers) and kept overnight inside a culture chamber at 18[degrees]C until the next day, when exposure experiments were conducted. The objective of keeping samples overnight at this temperature (close to the mean yearly value) was to maintain a 'common basis' for evaluating photochemical performance in the exposed samples. Otherwise, inter-seasonal comparisons would be complicated by different rates of enzymatic processes occurring under a broad range of in situ temperatures as commonly found in the study area. While this pre-acclimation might have slightly affected the initial fluorescence, it did not have any evident influence on the species composition (as observed microscopically) or on the photochemical responses at noon (which we used here). Therefore we reached a compromise between the comparability across seasons, and the representation of the natural community of plankton throughout the year, probably de-coupling to a certain extent our results from actual conditions in the lake. Exposure experiments were carried out as follows: Water samples were dispensed into 50-mL, UVR-transparent quartz tubes and exposed outdoors under solar radiation. Three radiation treatments were implemented (duplicate samples for each treatment): a) P (samples receiving only PAR, 400-700 nm): tubes wrapped with Ultraphan 395 filter (UV Opak, Digefra; 50% transmittance at 395 nm), b) PA (samples receiving PAR + UVA, 320-700 nm): tubes wrapped with Ultraphan 320 (Montagefolie No. 10155099, Folex, 50% transmittance at 320 nm), and c) PAB (samples receiving full solar radiation, i.e., PAR + UVA + UVB, 280-700 nm): tubes without any filter. The spectra of the filters/materials are published in Figueroa et al. (1997). The samples were then incubated during the whole day, inside a water bath to keep homogenous temperature in all samples (18[degrees]C [+ or -] 2[degrees]C). Both at the beginning (9:00 h) and at the end of the exposure (17:00 h), and also every hour, fluorescence was measured to evaluate changes in the effective photochemical quantum yield (Y) as follows: a sub-sample was transferred to a 5-mL quartz cuvette, where fluorescence variables were measured in vivo using a portable pulse-amplitude modulated fluorometer (Water-PAM, Walz, Germany). To obtain the Y of cells, the instantaneous maximal fluorescence ([F'.sub.m]) and the steady state fluorescence ([F.sub.t]) of light-adapted cells were measured using a saturating white light pulse (~5300 mol photons [m.sup.-2] [s.sup.-1] in 0.8 s) in the presence of a weak actinic light. Then Y was calculated after Van Kooten & Snel (1990) and Genty et al. (1989) as:

Y = ([F'.sub.m] - [F.sub.t])/[F'.sub.m] = [DELTA]F/[F.sub.'m]

The decrease of Y measured at 13:00 h (solar noon) was used here as a cumulative indicator of the effect of the exposure to solar radiation during the morning (i.e., between 9:00 and 13:00 h, local time) at each wavelength interval. This is presented here as an estimation of photo-inhibition (i.e., Y in the PAB and PA treatments relative to that in the P control) over the incubation period, and it was calculated as:

Decrease of Y by UVB (%) = 100 [([Y.sub.P] - [Y.sub.PAB]) - ([Y.sub.P] [Y.sub.PA])]/[Y.sub.P] = 100 ([Y.sub.PA] - [Y.sub.PAB])/[Y.sub.P] Decrease of Y by UVA (%) = 100 [([Y.sub.P] - [Y.sub.PA])]/[Y.sub.P] where [Y.sub.P], [Y.sub.PA] and [Y.sub.PAB] are the photochemical quantum yield of samples in the P, PA and PAB treatments, respectively.

Attenuation of solar radiation in the water column

Due to the lack of a small instrument to measure underwater radiation in such shallow eutrophic waters as those of Lake Cacique Chiquichano, the attenuation coefficient of PAR was estimated from chlorophyll and absorption measurements of the water column using published models derived from Branco & Kremer (2005) and Morris et al. (1995) for freshwater bodies with high chl-a and low penetration of radiation--see Goncalves et al. (2007) for a detailed description. Total attenuation of PAR in this case can be considered to be a result of particulate (phytoplankton chlorophyll) and dissolved chromo phoric organic matter (CDOM). Each of these contributors may be estimated separately. Microscopic observations did not reveal any significant amount of inorganic particulate material in the samples, so we considered that their influence in the attenuation of solar radiation was negligible over the sampling period, and thus it was not included in the calculations. Briefly, the absorption coefficient at 320 nm (using distilled water as blank), [a.sub.320], was calculated following Osburn & Morris (2003) as:

[a.sub.320] = 2.3 03 [DO.sub.320] [L.sup.-1]

where [DO.sub.320] is the optical density at 320 nm of a 10-mL of filtered (Whatman GF/F) water sample, measured using a diode-array spectrophotometer (Hewlett Packard 8453E), and L is the optical path of the cuvette (0.05 m). The contributions of chl-a ([micro]g [L.sup.-1]) and CDOM ([a.sub.320]) to the attenuation coefficient were then calculated as:

[K.sub.chl-a] = 0.22 + 0.008 chl-a + 0.054 [chl-a.sup.0.66]

[K.sub.CDOM] = 0.1948 [a.sub.320] - 0.9203

Finally, the attenuation coefficient for PAR ([K.sub.PAR]) was estimated as the sum of the contributions of individual components in the water as [K.sub.PAR] = [K.sub.chl-a] + [K.sub.CDOM].

Solar radiation and other meteorological variables

Surface solar irradiance was obtained with a broadband ELDONET filter radiometer (Real Time Computer, Mohrendorf, Germany) which measures (once a minute) energy in the UVB (280-315 nm), UVA (315-400 nm) and PAR (400-700 nm) wavebands. The radiometer is permanently installed on the roof of the Estacion de Fotobiologia Playa Union (EFPU) where the exposure experiments were carried out. Daily solar exposure was calculated based on surface irradiance measurements. Meteorological variables such as wind intensity/direction and temperature were recorded automatically every 10 min using a meteorological station (Oregon Scientific WMR-918) permanently installed on the roof of the EFPU building. Surface water temperature was recorded in situ using a digital thermometer.

Data treatment and statistic analyses

For the determinations of Y, the average of five consecutive fluorescence measurements was used as representative of each sample. All radiation treatments were done in duplicate, so the mean and half-mean range was calculated for each treatment. A repeated ANOVA test was used to establish differences among radiation treatments. A multiple linear regression analysis was also used to explain the variability observed in UVR-induced inhibition of Y. A significance level of 5% was used in all linear regressions and analysis.

RESULTS

Physical variables

Daily values of incident PAR varied throughout the year (Fig. 1a) between 0.1 and 12 MJ [m.sup.-2]. Daily UVB varied accordingly, with relatively low values during winter and high during summer, ranging between 0.18 and 50 kJ [m.sup.-2]. Average wind speed ranges (Fig. 1b) were within the historical values and trends (Helbling et al., 2005) i.e., the historical daily mean speed values were (mean (SD)): 5.1-21 (0.70), 3.95 (0.41), 4.10 (0.53), and 5.16 (0.55) m [s.sup.-1] for summer, autumn, winter and spring, respectively. Maximal wind speeds for the four days prior to sampling were, on average, between 7 and 20 m [s.sup.-1]. The relative contributions of chromophoric dissolved organic matter (CDOM) and chl-a to the attenuation of underwater radiation in the water column are shown in Fig. 1c. The diffuse attenuation coefficient for PAR ([K.sub.PAR]) varied between 2 and 13 [m.su.-1] with high values in February, April and August. It was thus determined that chl-a had stronger influence on [K.sub.PAR] than CDOM, resulting in relatively high attenuation of solar radiation during autumn and at the end of winter. Based on these [K.sub.PAR] values, the depth of the euphotic zone (i.e., 1% of surface PAR) varied between 0.35 and 2.3 m during the year (data not shown). It should be noted that inorganic particulate concentration was negligible in samples as assessed by microscopic observation of 24 h-settled samples. The lake also showed annual variations in surface temperature--between 24 and 4[degrees]C (Fig. 1c) with a mean yearly value of ~16[degrees]C.

Chlorophyll-a and zooplankton abundance

Total chl-a concentration during the study period (Fig. 2a) had three clear peaks--late February, April and August. The maximum chl-a (799 [micro]g [L.sup.-1]) was measured in August whereas relatively low values (4-55 [micro]g [L.sup.-1]) were determined during June an d in the period September to December. The chl-a concentration in the pico-nanoplankton fraction accounted for the bulk of total chl-a during almost the whole year (Fig. 2a). From January to April however, microplankton cells were relatively more abundant but pico-nanoplankton still accounted for 50% or more of the total chl-a. In regard to zooplankton abundance, the cladoceran D. spinulata and the copepod M. mendocinus showed alternated dominance (Fig 2b) except during the autumn-winter period, when the abundance of both groups was very low (e.g., Julian days 126 and 153). Highest abundances were ~400 and ~200 ind [L.sup.-1], for D. spinulata and M. mendocinus, respectively.

[FIGURE 1 OMITTED]

[FIGURE 2 OMITTED]

Phytoplankton abundance and dominance

The phytoplankton community (Fig. 3) was characterized by periods of presence and absence of Cyanophyta groups (i.e., cyanobacteria). On the other hand, when cyanobacteria was absent or accounted for less than 2% of the total cells, Bacillariophyta (i.e., diatoms) appeared to dominate the community, while Chlorophyta (i.e., green algae) varied with no visible pattern. This allowed us to separate the year into four periods based on the taxonomic composition of the samples: Cya1-Cya2 (samples/periods with dominance of cyanobacteria) and Dia1-Dia2 (samples/ periods in which diatoms dominated), with cyanobacteria and diatoms dominating in total about half of the year each. For some variables, especially species richness, it was not possible to assign only one of these groups (e.g., when the contribution of cyanobacteria and diatoms was similar) therefore some degree of overlapping is present in our calculations (e.g., the last points of the period Cya1 are also the first points of the period Dia1). Moreover, cyanobacteria and diatom abundances were negatively correlated ([R.sup.2] = 0.59; P < 0.01). Cyanobacteria (Fig. 3a) dominated mostly during summer and winter (although in some samples they co-occurred with green algae and diatoms). Diatoms (Fig. 3b) dominated during autumn and spring; in this group green algae (Fig. 3c) shared an important fraction in some samples, with cyanobacteria having little or no influence. Total cyanobacteria proportion (Fig. 3a) ranged from 0 to 99%, with two maximum values: 82% and 99% in Julian days 56 (summer, Cya1) and 259 (winter, Cya2) being Microcystis sp. and Synechocystis sp. the most important representatives in each period. Diatoms abundance varied with a similar null-to-full dominance of the community (Fig. 3b) and three times during this study they accounted for approximately 100% of cells: On Julian days 153 (autumn), 272 and 300 (spring). Navicula sp., Cyclotella sp., Surirella sp. and Nitszchia sp. varied throughout the year, although the two latest were most conspicuous in the autumn and spring maximum abundance of diatoms, respectively (Dia1 and Dia2). Green algae (Fig. 3c) did not exceed ~70% of the community, and their variations showed no clear pattern during the year. Maximal values of species richness (S, Fig. 3d) were observed in early autumn and in winter (S = 21 and S = 20 in April and August, respectively), whereas the minimum was observed during Autumn (S = 2 in June).

Representative phytoplankton taxa from Lake Cacique Chiquichano are shown in Table 1. Cyanobacteria-dominated samples were characterized by Microcystis spp., Synechocystis sp. and Lyngbya sp. whereas Navicula spp., Nitzschia sp., Cyclotella sp. and Surirella sp. were the most abundant species during diatom-dominated periods. Chlorophyceae (e.g., Oocystis spp. and Scenedesmus spp.) were frequently found year-round with different shares. The class Dinophyceae was poorly represented during the whole year and the only species present was Peridinium sp. Finally, only few Euglenophyta cells were observed during February and August (Trachellomonas sp. and Euglena sp., respectively).

Phytoplankton-zooplankton interactions

There were significant positive correlations between total chl-a concentration and the number of phytoplankton species present in the community during the Cya1 and Cya2 periods, meaning that the peaks of abundance were co-dominated by various species (Fig. 4a). No significant relationships (i.e., S versus chl-a) were observed during the periods of diatom dominance. In turn, during Cya1 and Cya2 periods, S was negatively correlated to the abundance of D. spinulata (Fig. 4b). Again, no significant correlations were established for the two periods of diatom domination. Finally, there were significant inverse correlations between D. spinulata dominance and both total phytoplankton chl-a and pico-nanoplankton chl-a fractions during the cyanobacteria-dominated periods (Fig. 4c). During Cya2 almost 100% of chl-a concentration was in the pico-nanoplankton fraction, so in Fig. 4c there is only one relationship for D. spinulata--chl-a during this period. On the other hand, no significant relationship was established between zooplankton abundance and chl-a during periods of diatoms dominance.

[FIGURE 3 OMITTED]

[FIGURE 4 OMITTED]

Photosynthetic responses of the phytoplankton communities

During all samplings, Y showed the typical daily pattern i.e., with Y decreasing significantly in all treatments towards noon and recovering partially or completely during the afternoon/evening (data not shown). However, when compared to samples receiving only PAR, Y at noon of those receiving full solar radiation were inhibited in most of the experiments. According to the composition of the phytoplankton community, this decrease of Y due to UVR showed a different relationship (Fig 5 a): UVR-induced inhibition of photosynthesis decreased with increasing proportion of diatoms whereas the opposite was found when cyanobacteria dominated the communities. In addition, UVR-induced inhibition was higher when more species were present during cyanobacteria-dominated periods (Fig. 5b) whereas the relationship was not significant when diatoms dominated.

Throughout the year, UVA and UVB inhibition varied significantly, with maximum values of 66 and 38% for UVA and UVB, respectively, but very low inhibition and even negative values were observed in some experiments (Fig. 6a). To further explore the variables accounting for UVR-induced inhibition, a relationship was established by means of a multiple linear regression in which the attenuation coefficient for PAR ([K.sub.PAR]), phytoplankton species richness (S), cyanobacteria abundance (Cya), Daphnia relative abundance (Daph) and UVR irradiance contributed for more than 92%:

Inh UVR = 2.109 [K.sub.PAR] + 0.764 S + 0.13 Cya + 0.226 UVR + 0.203 Daph

[FIGURE 5 OMITTED]

The modeled and observed UVR inhibition throughout the year (Fig. 6b) showed a generally good agreement with the observed values ([R.sup.2] = 0.92; P < 0.01), with UVR-induced inhibition increasing with increasing [K.sub.PAR], S, Cya, and UVR.

[FIGURE 6 OMITTED]

DISCUSSION

Lake Cacique Chiquichano is clearly subjected to seasonal changes in physical (wind, temperature, solar radiation) and biological (plankton community composition and abundance) variables. According to our estimations, the underwater optical environment is characterized as one of reduced penetration of solar radiation, especially during periods of high chl-a (Fig. 1c) as seen in other studies carried out in eutrophic lakes on the northern Great Plains (Arts et al., 2000). However, in this study we found that the periods of reduced penetration of solar radiation alternated with contrasting 'clear waters periods' (CWP, Fig. 1c) during which the euphotic zone encompassed almost the whole water column (Goncalves et al., 2007). It could be argued that seasonal changes in wind-driven re-suspension of benthic algae and inorganic particulate may be partially responsible for the observed seasonal patterns. However, microscopic observation did not reveal significant amounts of them in the samples. In addition, wind intensity (Fig. 1b) during the days previous to sampling was rather similar and high, and without a clear trend throughout the year. This allowed us to consider that the water column was well mixed all year round, and that if small amounts of wind-driven re-suspension of particulates occurred, this might have resulted in a very small underestimation of the attenuation of solar radiation. Furthermore, the magnitude of wind induced re-suspension of particles is likely to be similar during the year, given the strong winds characteristic in the study area (Fig. 1c). We are aware that wind-driven re-suspension of particulates may be a factor to consider when studying shallow lakes, where it may cause regular 'injections' of particles from the bed (Arfi & Bouvy, 1995). For example, Carrick et al. (1993) found wind re-suspension to be an important variable influencing the phytoplankton chl-a changes of shallow, productive Lake Apopka, Florida (USA). They argued that wind-induced mixing brought up phytoplankton from the lake bottom to the surface water column where the irradiances of the surface layers stimulated growth. However, and although solar radiation and temperature were most likely not limiting factors the authors stated that grazing might had influenced phytoplankton dynamics.

Our results suggest a top-down control of phytoplankton, most likely with D. spinulata as the main grazer, capable of significantly decreasing the chl-a in the water column (Fig. 4c) and thus modifying the water column optical characteristics (Fig 1c). Although our experiments were not designed to calculate ingestion rates of D. spinulata, we inferred grazing pressure from D. spinulata abundance. This is supported not only by the well-known grazing capability of Daphnia, due to potential high clearance rates and fast population growth rates (Hebert, 1978; Boersma, 1997; Lampert & Sommer, 1997) but also by the negative relationship between this cladoceran and chl-a concentration (Fig. 4c). Although in this study we did not intend to obtain grazing rates, estimations of pigments from Daphnia absorption spectra revealed high chl content (ca. 3 [micro]g per mg of Daphnia dry weight) in the cladoceran, therefore supporting the idea of a strong feeding pressure of the cladocerans on phytoplankton. It is arguable that by removing chl-a from the water, D. spinulata may have contributed to induce periods of increased penetration of radiation into the water column (Lampert & Sommer, 1997; Williamson et al., 2007). Indeed, this seems to be the case in our study site, as chl-a was the variable that contributed for most of the attenuation of solar radiation in the water column (Fig. 1c); thus when the cladoceran population exerted a strong grazing pressure over the phytoplankton community a CWP period was determined, as it seems to be a common pattern in many South American lakes (Echaniz et al., 2006). Interestingly, plankton dynamics seemed to be regulated mainly by the presence and abundance of D. spinulata but instead, there was no clear relationship between M. mendocinus and the phytoplankton species present in the lake.

Not only phytoplankton abundance (estimated using chl-a concentration) but also S was significantly affected by the presence of D. spinulata (Fig. 4). However, its presence was significant only when cyanobacteria dominated the phytoplankton assemblages (i.e., Cya1 and Cya2, Figs. 4b, 4c) that were also the periods that coincided with high chl-a concentration (Fig. 4a). This is in agreement with the findings of Van Gremberghe et al. (2008) that reported that in general, the zooplankton community composition (especially the cladoceran community) was more important in structuring the cyanobacterial community than the total zooplankton biomass was. Particularly, previous studies (Oberhaus et al., 2007) have reported the ability of the genus Daphnia to graze on cyanobacteria including Microcystis (Van Gremberghe et al., 2008). Thus one can speculate that without the strong grazing pressure of D. spinulata on the phytoplankton community, Lake Cacique Chiquichano would mostly be a typical "ever-green" eutrophic lake during the whole year, with very low penetration of solar radiation into the water column and a high number of cyanobacteria species. However, this was not the case, and moreover, we postulate that the abundance of D. spinulata modulated not only the phytoplankton community, but also indirectly affected the observed photosynthetic responses of phytoplankton.

During the study period, cyanobacteria and diatoms alternated their dominance, as previously observed in other eutrophic waters (Watson et al., 1997). Cyanobacteria dominated during the 'low transparency' phase in the lake, while diatoms dominated during the CWP (Figs. 1 and 3). The general photosynthetic response throughout the study period was of UVR-induced photo-inhibition increasing with increasing proportion of cyanobacteria in the samples (Fig. 5a) and with increasing number of species (Fig. 5b) for both Cya1 and Cya2 periods. In principle, it may seem strange that inhibition increased when more phytoplankton species (and more chl-a) were present. However, this was most probably due to a selection towards few and more resistant species with increasing D. spinulata abundance and increasing UVR exposure. In both Cya-periods, D. spinulata may have grazed on pico-nanoplankton cells (Fig. 4c) decreasing also the number of species (Fig. 4b). It has been shown in previous studies (Helbling et al., 2001b) that small cells are less sensitive to UVR than larger cells are, when addressing effects on photosynthesis. In our study, however, we can not rule out one of these possibilities (i.e., if the species were mostly affected by UVR) and then grazed by D. spinulata, or if the ingestion of these small cells was independent of UVR. D. spinulata might have fed less on relatively larger cells, which started to acclimate to higher irradiances (because of the increasing transparency of the water column) and thus became less sensitive. Therefore, and in this case, the process would be an indirect effect of grazing on the observed photo inhibition.

The fact that during periods of high proportion of cyanobacteria the community had higher photosynthetic inhibition values could be simply the result of cells being acclimated to low underwater radiation conditions during the "high attenuation" period. This is in agreement with a comparative study carried out in the Andean lakes that showed that phytoplankton in "high-attenuation" lakes had higher damage and inhibition of photosynthesis than in clear lakes (Villafane et al., 2004b) being the high sensitivity associated to their previous acclimation to low radiation levels. In fact, previous studies carried out in Lake Cacique Chiquichano (Klisch et al., 2005) have reported a high sensitivity towards UVR (as assessed through DNA damage) in summer populations (i.e., dominated by cyanobacteria). It should be noted though that some cyanobacteria are considered to be resistant to UVR because of their ability to synthesize UV-absorbing compounds (Sinha et al., 2001b) that act as sunscreens and thus protect cells against UVR stress, while others seems to acquire resistance by changing their morphology (Wu et al., 2005). Particularly, the genera Synechocystis and Microcystis--which were important members of the Cyanophyta community in Lake Cacique Chiquichano (Table 1), are known to produce UV-absorbing compounds (Liu et al., 2004; Zhang et al., 2007) however, in our study we did not register any significant amount nor a relationship between these potential protective compounds and cyanobacteria abundance throughout the year. In contrast to the response of cyanobacteria, UVR-induced inhibition decreased with increasing dominance of diatoms (Fig. 5a). In fact, diatoms seems to be more resistant to UVR as compared to other groups probably because of their silica "protection" as suggested by Wulff et al. (2008) or by the synthesis of UV-absorbing compounds as demonstrated for other environments (Helbling et al., 1996), although this latter option did not appear to be the case. It could also be possible that diatoms displayed a high rate of repair, as also seen in marine environments of the Patagonian coast (Helbling et al., 2001a) but this hypothesis remains to be tested for Lake Cacique Chiquichano assemblages.

In regard to the relative proportions of UVA- and UVB-induced photo-inhibition, it was seen that although it was variable throughout the year, UVA accounted for most of the share (Fig. 6a) as it is the common response in natural waters (Villafane et al., 2003); however, there were some dates in which UVB-induced inhibition was similar to that of UVA, as also observed in marine assemblages of Patagonia (Villafane et al., 2004c). Moreover, there were some periods of complete diatom domination in which UVR even stimulated photosynthesis (Julian day 300, Fig. 6b) as also seen under low radiation (Barbieri et al., 2002) or fast mixing conditions (Helbling et al., 2003). Overall, the multiple linear regression model explained great part of the variability (i.e., 92%) based on D. spinulata and cyanobacteria abundances, species and underwater attenuation of radiation. This latter parameter denotes the influence of CDOM and most importantly of Chl-a absorption in the final [K.sub.PAR]. Weighting the causes of the species' replacements (e.g., radiation-induced photo-inhibition versus the modification of community due to grazing) probably remains to be further elucidated. It is not clear if UVR affects phytoplankton and then it is easily eaten by D. spinulata, or if there is a selective feeding on some species leaving more resistant ones in the way.

Changes in phytoplankton structure or taxonomic composition have been investigated in other lakes before (considering grazing or not). However, little attention was paid in considering the indirect effects of common grazers on photosynthetic responses to solar radiation of natural communities occurring throughout the seasonal cycle, as we reported in this study. Overall, our results indicate that both solar radiation and grazing may affect the natural phytoplankton of Lake Cacique Chiquichano. Grazing pressure would contribute to shape the taxonomic composition of phytoplankton in this lake, driving different effects on the photosynthetic performance of the community according to the dominant group present at that time. It remains to be tested however, if the pattern observed in our results is typical for this kind of lakes (i.e., shallow, eutrophic waters but with a periodic occurrence of a CWP) and if our results can be generalized to water bodies with similar characteristics. Simultaneous, parallel experiments of grazing rates and selectivity would add more quantitative data on the role of grazing pressure, and it would be the next logical step triggered by the results of the present study.

DOI: 10.3856/vol39-issue1-fulltext-11

ACKNOWLEDGMENTS

This work was supported by Agencia Nacional de Promocion Cientifica y Tecnologica--ANPCyT (PICT2005-32034 and PICT2007-01651), Consejo Nacional de Investigaciones Cientificas y Tecnicas (PIP2005-5157) and Fundacion Playa Union. We thank the comments and suggestions of two anonymous reviewers that contributed to improve our manuscript. This is Contribution No. 121 of the Estacion de Fotobiologia Playa Union.

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Received: 14 May 2010; Accepted: 30 December 2010

Rodrigo J. Goncalves (1), Virginia E. Villafane (1), Cesar D. Medina (2), Elena S. Barbieri (2) & Walter E. Helbling (1)

(1) Estacion de Fotobiologia Playa Union, Casilla de Correo 15, 9103 Rawson, Chubut, Argentina

(2) Consejo Nacional de Investigaciones Cientificas y Tecnicas, Argentina

Corresponding author: Rodrigo Goncalves (rodrigo@efpu.org.ar)
Table 1. Representative phytoplankton groups on samples collected
at Lake Cacique Chiquichano during the study
period.

Tabla 1. Grupos representativos de fitoplancton presentes en la
Laguna Cacique Chiquichano durante el periodo de
estudio.

Cyanophyceae         Chlorophyceae

Anabaena sp.         Actinastrum sp.
Lyngbya sp.          Ankistrodesmus sp.
Merismopedia sp.     Botryoccocus sp.
  1, sp. 2
Microcystis sp.      Closterium sp.
  1, sp. 2           1, sp. 2
Pseudoanabaena sp.   Coelastrum sp.
Synechocystis sp.    Kirchneriella sp.
Oscillatoria sp.     Oocystis sp.1,
                     sp. 2
                     Pediastrum sp.
                     1-sp. 4
                     Scenedesmus sp.
                     1-sp. 9

Bacillariophyceae   Dinophyceae

Achnanthes sp.      Peridinium sp.
Cocconeis sp.
Cyclotella sp.

Cymbella sp.

Gyrosigma sp.       Euglenophyceae
Hantzchia sp.       Euglena sp.
Navicula sp.        Trachellomonas
1, sp. 2            sp.
Nitzschia sp.

Surirella sp.
Synedra sp.
Ulnaria sp.
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Title Annotation:Research Article
Author:Goncalves, Rodrigo J.; Villafane, Virginia E.; Medina, Cesar D.; Barbieri, Elena S.; Helbling, Walte
Publication:Latin American Journal of Aquatic Research
Article Type:Report
Date:Mar 1, 2011
Words:7875
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