Introduction

Although Polar Regions benefit from continuous sunlight conditions during the summer, the long, near-aphotic winter period results in the lowest annual levels of photosynthetically active radiation (PAR) at the surface of the Earth (Campbell and Aarup 1989; Larcher 2001). This, together with the presence of ice (and snow) covers most of, or all through, the year (Vincent et al. 1998; Fritsen and Priscu 1999) greatly restricts the light regime of polar lakes. Antarctic lake environments are further considered as extremely low productive ecosystems because of their oligotrophic situation and the low temperatures to which they are constantly exposed. Thus, a common belief is that the growth stage of phototrophs in continental Antarctic lakes (phytoplankton and benthic algae are the main primary producers in these lakes) can take place only during the summer.

Due to logistic difficulties, many ecophysiological studies of algal communities in Antarctic lakes are carried out in summer and spring period, although the year-round phytoplankton dynamics studies conducted in some continental Antarctic lakes, at Crooked Lake (68°35′S, 78°25′E; Bayliss et al. 1997; Henshaw and Laybourn-Parry 2002), at Watts Lake (68°36′S, 78°13′E; Heath 1988) in the Vestfold Hills, and at West Ongul Ô-ike Lake (69°01′S, 39°35′E; Ohyama et al. 1990, 1992) on the Sôya Coast. No obvious seasonal changes in biomass were reported at Crooked Lake (Bayliss et al. 1997) but the phytoplankton populations of Watts and Ô-ike lakes were shown to reach a peak in spring (Heath 1988; Ohyama et al. 1990, 1992). Similar spring increases in phytoplankton biomass and production under subsurface waters were reported in oligotrophic deep lakes and some saline meromictic lakes (Lizotte et al. 1996; Bell and Laybourn-Parry 1999). On the other hand, phytoplankton blooms in summer were reported in maritime Antarctic lakes (Butler 1999; Butler et al. 2000), and meta- and hypolimnion in meromictic lakes (Bell and Laybourn-Parry 1999; Henshaw and Leybourn-Parry 2002). These results, however, should be taken with care since these studies consisted of only selective measurements (once or twice a month) and cannot, therefore, deliver detailed information about the seasonal dynamics in the environment of these lakes.

Recently, challenges of continuous measurements of limnological parameters, such as underwater light climate and temperature in Antarctic lakes, were tried (Fritsen and Priscu 1999; Palethorpe et al. 2004), and revealed the dynamics that occurred under ice cover. However such information are still limited in few lakes.

To remedy this situation, we monitored continuously from January 2004 to February 2005 several physical and biological parameters of the two lakes from the Skarvsnes area on the Sôya Coast, using a suite of time-data recording instruments that measured water temperature, chlorophyll a concentration, turbidity, and PAR. These monitoring systems were complimented by a weather observation station that measured solar radiation, wind speed and air temperature in the Skarvsnes area. We discuss the seasonal patterns of occurrence of phytoplankton in freshwater lakes as chlorophyll a fluorescence signals, with special emphasis on the observation of blooming events during the cold and dim periods of the year.

Materials and methods

Study sites

On the southern part of Sôya Coast, near Syowa station (69°S, 39°E), East Antarctica (Fig. 1), ice-free areas and islands appeared about 20,000 years ago under the retreat of glacier and the influence of iso-static uplifts that occurred after the last major glaciations (Miura et al. 1998). Areas currently < ca. 20 m above sea level were previously sea bed (Miura et al. 1998). Consequently, lakes are found in great number on the Sôya Coast and they present a remarkable diversity of sizes, shapes, and limnological properties (Imura et al. 2003). The Skarvsnes area (69°20′S, 39°36′E), located on the eastern shore of Lützow-Holm Bay, is one of the widest ice-free area of the Sôya Coast (Fig. 1) and contains >50 freshwater to hyper saline lakes. In the present study, we selected the following two freshwater lakes for our experiments (Fig. 2): Oyako-ike (area 48,000 m2; maximum depth 8.0 m; altitude 5 m), one of marine-relic lakes, and Hotoke-ike (formerly known as “B-4”) (area 6,000 m2; maximum depth 3.0 m; altitude 120 m). Previous studies have investigated the physical properties (Imura et al. 2003) and geological histories (Matsumoto et al. 2006) of several lakes from the Sôya region, as well as the eco-physiology of the lacustrine mosses found in some of them (Kudoh et al. 2003a, b, c).

Fig. 1
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Locations of the study area and lakes

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Fig. 2
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Landscape of Lake Oyako-ike and Lake Hotoke-ike in summer

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Methods

The meteorological station (KADEC-Me, KONA system) was installed in the center of the Skarvsnes area, on the shore of Lake Suribati. The station automatically recorded the solar radiation (wavelength 305–2800 nm), wind speed, and air temperature every 30 min from March 2004 onwards.

Seasonal changes in limnologic parameters were monitored continuously using mooring arrays installed in the centers of lakes Oyako-ike and Hotoke-ike (Fig. 3). The system at Lake Oyako-ike comprised three temperature loggers (NWT-SN, Nichiyu Giken Kogyo), a chlorophyll fluorescence meter with turbidity logger (ACLW-CMP, Alec) and a PAR logger (MDS type-L, Alec). The system at Lake Hotoke-ike consisted of only the fluorescence/turbidity recorder and the PAR meter. The loggers sampled data every 10–60 min. With such a setting, data were collected for more than a year. All loggers were pre- and post-calibrated by the manufacturers, who found no significant drifts in the measurements over the course of the study.

Fig. 3
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Illustration of the mooring system installed in a Lake Oyako-ike and b Lake Hotoke-ike

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Loggers were placed at specific depths (see Fig. 3), while the upper plastic floats were placed at 1.8–2.0 m, i.e. deeper than the maximum depth at which ice forms in winter. Mooring arrays were installed on January 2004, and retrieved on February 2005 using an inflatable raft.

In order to verify the accuracy of the instruments, we measured manually the water temperature, turbidity, salinity, pH, dissolved oxygen (DO), and PAR intensity at the times when the moorings were installed and retrieved. Manual measurements were performed at the centers of the lakes with a multichannel water quality meter (WQC-22A, TOA-DKK) and a PAR sensor (193SA, Li-Cor). An additional measurement was done in early spring (September) through a hole drilled into the ice covering, Lake Oyako-ike. The water samples, collected 3 m under the surface of the lake by a Kitahara-type cylindrical water sampler (1 L capacity), were concentrated onto GF/F glass fiber filters, and extracted by the N,N-dimethylformamide method (Moran and Porath 1980). The concentration of extracted chlorophyll a was determined using a fluorometer (10-AU, Turner Design) against a sample of pure chlorophyll a. The chlorophyll fluorescence signals from the mooring instruments were converted into chlorophyll a concentrations using the extracted chlorophyll a data, as, ((chlorophyll a concentration) = 0.45 × (fluorescence readings) + 0.26). The chlorophyll a data (every 60 min) were, then, summarized for 1 day interval and averaged, in order to cancel the diurnal fluctuation of the chlorophyll fluorescence.

Results

Meteorological data

Solar radiation followed clear diurnal cycles and also varied on a day-to-day basis with weather conditions (Fig. 4). Overall, solar radiation gradually decreased until the beginning of winter (May), was virtually null during the 103 days of the polar winter (May–mid-August) and gradually increased after mid-August to reach a maximum of ca. 900 W m−2 at noon on a mid-summer (December) fine day. Daily-integrated radiation also showed diel fluctuations and the maximum value was observed in late December (35.6 MJ m−2 day−1). Prolonged periods of low radiation were observed in March and September–October, corresponding to bad weather (cloudy, overcast, storm events) events that followed one another at several-day intervals. In addition, such bad weather periods lasted longer in autumn and spring compared to other seasons.

Fig. 4
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Solar radiation monitored on the shore of Lake Suribati (grey dashed line) and the corresponding daily-integrated value (black line)

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Annual variations in air temperature followed a bell-shaped distribution similar to that of the solar radiation. Temperatures in early March were occasionally >0°C but always <0°C between April and the beginning of October (Fig. 5). The range of temperature fluctuation was greater in winter than in any other seasons (from ca. 0 to −40°C). In winter, warm temperatures were recorded during periods of low solar radiation, as well as during periods of strong winds (speeds > 20 m s−1, Fig. 6), i.e. during blizzards. Temperatures >0°C were frequently observed in late November. Temperatures subsequently remained positive from mid-December till early January (a period of snow and ice melting). Radiation and air temperature data averaged over each month are presented in Table 1.

Fig. 5
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Air temperature monitored on the shore of Lake Suribati

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Fig. 6
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Maximum wind speed monitored on the shore of Lake Suribati

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Table 1 Daily-integrated value of solar radiation and air temperature (monthly average, SD and range) recorded on the shore of lake Suribati from March 2004 to January 2005
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Limnological data at Lake Oyako-ike

The salinity in the water column of L. Oyako-ike was 0.02% in January when water column was vertically well mixed (no thermally stratified), pH was 8.0 ± 0.2 and DO was 15.9 ± 0.3 mg L−1.

From January to early March, the water temperatures at 2.8 and 5.0 m in Lake Oyako-ike followed similar decreasing trends but they fluctuated more than the temperature recorded at 7.5 m during the same period. All temperatures reached a minimum of 0°C in early March before increasing again until the end of March. From early March, the amplitude of the temperature fluctuations became smaller as ice covered the surface of the lake. Note the abrupt spike observed in the turbidity signal in the beginning of March (Fig. 7), which suggests that ice nucleation occurred in the water column. A clear inverse-thermal stratification was observed from late March to early October. All temperatures started to rise rapidly from mid-October following the sudden augmentation of light penetration into the water (cf. Fig. 8). The near-surface water (2.8 m) temperature decreased during December and was accompanied by an increase in the turbidity that probably resulted from a supply of melt-water from the catchments. It also suggests that there was a layer of much cooler water just underneath the ice cover. In late December, water temperatures showed large diel fluctuations, with the upper temperature signals (2.8 and 5.0 m) following similar trends again.

Fig. 7
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Seasonal changes in the temperatures of the top (2.8 m), middle (5.0 m), and bottom layers (7.5 m) of the water column, as well as in the turbidity recorded at 3.0 m depth in Lake Oyako-ike

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Fig. 8
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Seasonal changes in daily PAR recorded at 3.8 m (a), and chlorophyll a concentration recorded at 3.0 m (b) in Lake Oyako-ike. The grey bars indicate the main period of phytoplankton growth

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The PAR at 3.8 m was initially >20 mol m−2 day−1, after which it fluctuated considerably, although still following an overall decreasing trend until early May (Fig. 8a). PAR values measured undetectable levels over 115 days of the winter period, until early August. In early August, the PAR crossed the detectable levels (>0.10 mol m−2 day−1) and gradually increased until early September (0.38 mol m−2 day−1), but the PAR showed a sudden decrease (<1/5th level) and the low-PAR period continued almost 1 month after that. The PAR in spring (September to October) showed such a sudden decrease and increase on several occasions, especially sudden increases coincided just after strong wind events (suggesting that light penetration was enhanced by the wind, blowing away the snow cover on the ice). Note the summer PAR values differed considerably between 2004 and 2005 due to attached algal growth on the photo sensor of the logger (we found this situation when we retrieved the moorings in 2005). Thus, all recordings in late 2004 and early 2005 are underestimated. To try and quantify this problem, we compared the PAR values collected manually (cf. “Materials and methods”) on the 7 September 2004 to those recorded by the logger and found that the logger PAR was 6–7 times smaller than the manually-collected PAR values at that time (Table 2).

Table 2 Vertical profile of the PAR (mol μm− 2 s− 1) with depth for Lake Oyako-ike, and the skylight at 11.15 AM on 7 September 2004
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Chlorophyll a concentrations gradually increased under the ice cover in autumn and slightly decreased during the dark winter (Fig. 7b). Under the dim-light conditions observed in August, chlorophyll a concentration augmented rapidly to reach >2 μg L−1 in mid-September, but this was followed by a sudden drop, concomitant to a rise in PAR levels (between 8 October and 5 November). In early November, chlorophyll a concentration peaked again before decreasing gradually as spring progressed. In January, the concentration in pigments reached its annual minimum in spite of the substantial amount of PAR in the water column.

Limnological data at Lake Hotoke-ike

The temperature and salinity in the water column of L. Hotoke-ike was 8.75°C and 0.15% in January when water column was vertically well mixed, pH was 7.2 ± 0.1 and DO was 13.8 ± 0.9 mg L−1.

Seasonal changes in PAR values and chlorophyll a concentration in the shallower Lake Hotoke-ike were comparable to those observed in Lake Oyako-ike; i.e. chlorophyll a increased under low PAR conditions in autumn and spring (Fig. 9). Autumnal increase of chlorophyll a was more rapid and larger than the spring increase. Similar to Lake Oyako-ike, drastic PAR increases were also observed in spring, probably in relation with the sudden disappearance of the snow on the ice cover mentioned previously (cf. above). Attached algal growth on the photo sensor of the logger was not found visually in L. Hotoke-ike when we retrieved the moorings in 2005.

Fig. 9
figure 9

Seasonal changes in PAR recorded at 2.2 m (a), and chlorophyll a concentration recorded at 2.0 m (b) in Lake Hotoke-ike. The grey bars indicate the main period of phytoplankton growth

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Peak values of chlorophyll a in autumn and spring were nearly the same and 1/4th levels of those observed in L. Oyako-ike, respectively.

Discussion

The present study reports the fine-scale seasonal changes, monitored over a year, of the limnological parameters of lakes Oyako-ike and Hotoke-ike, two typical oligotrophic, shallow, freshwater lakes along the Sôya Coast ice-free area (Imura et al. 2003) in East Antarctica. Our results confirmed the presence of water in liquid phase under the Skarvsnes ice-covered lakes during the middle of Antarctic winter, as the water temperature recorded during this period ranged from 0 to 10°C. The ice-cover period lasted about 11 months, from the end of February 2004 until January 2005. Water temperature under the ice increased in autumn and spring, and reached up to 10°C before complete ice melting. The symmetrical evolution of the temperatures recorded at 2.8 and 5.0 m depths in summer is indicative of vertical mixing induced by both wind action and thermal convection during periods of open water. In contrast, the winter inverse-thermal stratification (April–October) suggests low turbulences.

Light penetration was also greatly affected by snow and ice covers, the influence of these two factors decreasing as season progressed towards the summer. Interestingly, the chlorophyll a concentration was at a minimum during the peak of light availability in summer when ice-cover melted away. The chlorophyll a concentration in mid-summer was even lower than that observed during the dark mid-winter period.

The possible reasons of the changes in chlorophyll a concentration at the depth where chlorophyll a-logger deployed were, simply phytoplankton growth/loss, physiological light-adaptation to PAR change, transportation of phytoplankton by vertical mixing events, sinking loss, positive movement by phototaxis and chemotaxis, or combination of those factors (e.g. Morgan-Kiss et al. 2006).

Increases in chlorophyll a in L. Oyako-ike occurred between March and April, August–September when water column was inversely stratified as expected water temperature data (Fig. 7). If phytoplanktons which possess swimming motility (e.g. flagellates) keep their vertical position as they favor (near the surface) during dim-light late autumn and early spring, then such phenomenon may make chlorophyll a increase at our chlorophyll a-logger. Following sudden PAR penetration in October in water-column induced vertical mixing, at least 5 m upper surface water (Fig. 7), and phytoplankton cells were diffused through the entire water column by the diurnal mixing event. But increase of chlorophyll a in early November, occurred under diurnal vertical mixing event. These may suggest only changes in water column stability and vertical migration of phytoplanktons are not enough reasons for chlorophyll a changes.

Sudden decrease of chlorophyll a occurred in October when PAR penetration increased, between two peaks of chlorophyll a in spring in L. Oyako-ike, may be the results of photo-inhibition or light adaptation of shade-adapted phytoplankton. Damages of shade-adapted phytoplankton under cold environment when they are exposed to strong light, or reduction of chlorophyll contents under strong light are well known (reviewed by Morgan-Kiss et al. 2006). Further studies are required for the evaluation of above hypotheses.

Spring growth of phytoplankton had already been reported elsewhere (Heath 1988; Ohyama et al. 1990; Laybourn-Parry and Bayliss 1996) and to explain such a paradoxical situation (growth under weaker light), it has been proposed that phytoplankton in East Antarctic lakes is well shade-adapted (Lizotte and Priscu 1992; Lizotte et al. 1996). A study conducted at Lake Bonney (78°43′S, 162°23′E), in the Taylor Valley, showed that chlorophyll a concentrations and rates of primary production in the whole water column (depth-integrated) were positively and linearly related, increasing as the season progressed towards the summer (Fritsen et al. 1999). This indicated PAR increase can enhance the phytoplankton biomass, if the water column is considerably deep and non-turbulent. However, the lakes in the Sôya Coast and L. Bonney are different, the latter is permanently ice-covered and the phytoplankton community never experiences the high irradiance values measured in our study lakes. Phytoplankton in the shallow and seasonally open-water lakes are directly exposed to high PAR in summer and cannot escape, because the water column is vertically well mixed by wind and thermal convection. Therefore, phytoplankton in present lakes may be easily damaged by strong light during summer. Henshaw and Laybourn-Parry (2002) reported chlorophyll a peaks in early spring at shallow basins, and a peak in summer at deep basin in East Antarctic lake. These seasonal differences in chlorophyll a peaks among different basins support the above interpretation.

In this respect, our continuous and simultaneous measurements of variations in light climate and phytoplankton biomass in the Oyako-ike and Hotoke-ike lakes demonstrated conclusively that phytoplankton hits a low concentration when light is at its highest level in mid-summer, if the present chlorophyll a concentration is assumed to the phytoplankton biomass. Moreover, we showed that chlorophyll a increase can be initiated with only little light penetration and that stopped immediately and turned to decrease when underwater light suddenly increased. For instance, in Fig. 8, chlorophyll a peaked on 8 October 2004 and then decreased drastically over the next several days, while the PAR simultaneously increased about four-fold from 8 October to the next day as the snow covering the ice was blown away by the wind. In other words, an increase in light penetration matched precisely with a decrease in chlorophyll a. This is not the sole example that we found in our data. Hence, similar changes in chlorophyll a in Lake Hotoke-ike correlated well with opposite fluctuations in the PAR climate (Fig. 9).

In general, situation of stress for plants can be caused by various factors, such as too strong or too weak light regimes, elevated or low temperatures, and rarity of nutrients (Kreeb 1974; Levitt 1980a, b; Larcher 2001; Falkowski and Raven 2007). As mentioned earlier, the annual growth period of phototrophs in Antarctic lakes is considered to be brief because of the specific light regime found under Antarctic latitudes, i.e. continuous daylight in summer and total absence of solar radiation during the long winter period. Moreover, the presence of ice for most of the year, as well as the characteristics of the ice and snow covers, have profound consequences on the light climate of lake waters (Howard-Williams et al. 1998; Fritsen and Priscu 1999).

It is commonly known that the higher the latitude, the longer the daylight and the greater the daily solar radiation (Lalli and Parsons 1993). For example, the monthly average daily solar radiation in December was 28.3 MJ m−2 day−1 in the Skarvsnes area (Table 1), while it is only 16.1 MJ m−2 day−1 in May in Tokyo (35°40′N, 39°45′E), a mid-latitude city (average from 1972 to 2000, Japan Meteorology Agency, http://www.jma.go.jp/jma/indexe.html). This example illustrates well the important amount of daily solar radiation that can be recorded at the ground level during the Antarctic summer. In the water column of L. Oyako-ike, the instantaneous PAR reached 500–600 μmol m−2 s−1 at 3.8 m depth around noon on clear day in summer. In this regard, the Antarctic summer, with its strong light regime, can be seen as extremely susceptible to the damage period for the photosynthesis of algae if they do not have enough light protection/regulation mechanisms.

Our study also revealed that the autumnal and spring phytoplankton blooms were different, as demonstrated by the different PAR levels observed in each season. In spring in L. Oyako-ike, the bloom started under faint light at 5 μmol m−2 s−1 of PAR (Table 2), while in autumn, the bloom began at larger PAR values of nearly daily maximum (at 113 μmol m−2 s−1, if it was a conservative estimate with fouling on the light sensor of the mooring system) at 11.00 AM. In L. Hotoke-ike, the spring bloom started at 5 μmol m−2 s−1, and the autumn bloom began at 440 μmol m−2 s−1 at noon. We, therefore, suggest that the autumn algal community may be adapted to much higher light levels which they experienced during summer, and that the spring one may be more shade-adapted than the autumn algal community.

Benthic algae is another important primary producer, especially in shallow oligtrophic Antarctic lakes (e.g. Vincent et al. 1993; Elliss-Evans et al. 1996; Tang et al. 1997; Sabbe et al. 2004). The benthic algae sometimes makes thick algal deposits over a few meters (Hodgson et al. 2001; Verleyen et al. 2003, 2004). Ecological success of the benthic algae, rather than phytoplankton, in shallow oligotrophic lakes may attribute to possess photo-protective or photo-regulative pigments that protect too bright and continuous solar radiation during summer (Vincent and Quesada 1994; Tang et al. 1997; Hodson et al. 2004). Heath (1988) pointed out the benthic algal production increased toward summer, while phytoplankton production in the same lake diminished. Phytoplankton in shallow lakes is easily exposed to much stronger solar radiation during ice-free summer period due to wind-induced vertical mixing, heat convection, and such situation together with oligotrophic condition, may induce photo-inhibition, and then, phytoplankton biomass could not increase in summer.

Our results suggest that light climate may be one of the key factors conditioning the development of lacustrine organisms in the Antarctic environment (Fritsen and Priscu 1999). The significant decrease in chlorophyll a concentration concomitant to the increase in light around mid-summer strongly augurs for the bright summer light to act as an inhibitor of the phytoplankton growth, whereas the faint winter light may represent the optimal condition for the development of Antarctic phytoplankton. Further analyses in this direction should help us elucidate the relationship between the light climate and survival strategies of primary producers in Antarctica.