Aquat Ecol (2010) 44:531–539 DOI 10.1007/s10452-010-9329-5
The vertical distribution and abundance of Gammarus lacustris in the pelagic zone of the meromictic lakes Shira and Shunet (Khakassia, Russia) Egor S. Zadereev • Alexander P. Tolomeyev • Anton V. Drobotov • Anna Yu. Emeliyanova • Mikhail V. Gubanov
Received: 20 May 2009 / Accepted: 20 May 2010 / Published online: 18 June 2010 Ó Springer Science+Business Media B.V. 2010
Abstract The vertical distribution and abundance of Gammarus lacustris in the pelagic zone of two fishless meromictic lakes, L. Shira and L. Shunet, in Southern Siberia (Russia), was studied with the underwater video recording system and using vertical hauls. In both lakes, during summer stratification, Gammarus was distributed non-homogenously, with a stable peak in the metalimnion. The average depth of Gammarus population in the pelagic zone was significantly correlated with the depth of the thermocline. Gammarus abundances obtained using vertical plankton hauls with net were quite comparable with those obtained from video records. The peak abundance of Gammarus in the pelagic zone of the lakes observed with underwater video amounted up to 400 individuals m-2, while the peak animal densities in the metalimnion reached 50 ind. m-3. The data are compared with previously published abundances of Gammarus in the littoral of Lake Shira. Both littoral and pelagic can be equally important habitats for
Handling Editor: R. D. Gulati. E. S. Zadereev (&) A. P. Tolomeyev A. Yu. Emeliyanova M. V. Gubanov Institute of Biophysics SB RAS, Krasnoyarsk, Akademgorodok, Russia 660036 e-mail:
[email protected] E. S. Zadereev A. V. Drobotov Siberian Federal University, Svobodnyi 79, Krasnoyarsk, Russia 660041
amphipods in meromictic lakes. The absence of fish in the pelagic zone, high oxygen concentration, low water temperature, increased seston concentration, elevated water density in the metalimnion and the anoxic hypolimnion can be the most probable combination of factors that are responsible for the peak of Gammarus in the metalimnion of these lakes. Keywords Meromictic lake Amphipod Gammarus lacustris Vertical distribution Thermocline
Introduction The amphipod Gammarus lacustris is generally considered as a benthic animal in lakes. The animals are concentrated predominantly in bottom waters. There is growing evidence suggesting that the ecological niche of Gammarus is not benthic but benthoplanktonic (Kelly et al. 2002; Wilhelm et al. 2000). Thus, Gammarus can be regarded not only as a benthic detritivore but rather as a predator that can have an effect on pelagic community (Wilhelm and Schindler 1999). Studies of pelagic communities in lakes are often focused on the vertical structure of the plankton, the vertical distribution of which reflects physiological, behavioral and ecological preferences of organisms. Lake Shira and Lake Shunet (Khakassia, Russia) are meromictic lakes (Zotina et al. 1999; Rogozin et al. 2009), where Gammarus is one of the
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few dominant species among zooplankton. Yemelyanova et al. (2002) have been shown that in Lake Shira the highest densities of Gammarus occur in sublittoral area. They also observed Gammarus in the pelagic zone of the lake, in densities much lower than in the littoral zone. Also, repeated zooplankton sampling and collection of sediments in central parts of these both lakes showed that neither G. lacustris nor other zooplankters occurred either in the anoxic monimolimnion or in the sediment. Thus, we can suggest that Gammarus lacustris occupies a benthoplanktonic niche in both lakes. Moreover, only a few authors reported observing G.lacustirs in the pelagic zones of different lakes (Matafonov 2007; Trevorrow and Tanaka 1997; Wilhelm et al. 2000), none of which are meromictic. Thus, even in the pelagic zone of these lakes, the bottom is habitable for Gammarus. In meromictic lakes, anoxic deeper layers restrict the vertical distribution of zooplankton (Zadereev and Tolomeyev 2007). It is this clear that in the pelagic zone of the meromictic lake there is no bottom habitat for benthic animals. The aim of our research was to study the vertical distribution and abundance of Gammarus lacustris in the pelagic zone of two meromictic lakes. We used underwater video recording system and the classical technique of taking vertical hauls and compared the Gammarus concentrations based on these two methods. The depth distribution thus obtained was compared with the vertical distribution of temperature, salinity, dissolved oxygen and seston concentrations.
Materials and methods Lake description Lake Shira is located (54°300 N and 90°110 E) in the northern part of Republic of Khakassia, Siberia. The maximum depth of Lake Shira is 23.4 m. The surface area of the Lake is 35.9 km2. The salinity of the water is 10.5 ppt in the epilimnion and 12.5 ppt in the anoxic hypolimnion. The depth of the upper boundary of the monimolimnion varies seasonally and annually between 11 and 15 m. Hydrogen sulfide concentrations in the Lake Shira monimolimnion vary from 20 to 30 mg L-1 (Rogozin et al. 2009). A general description of the lake ecosystem was
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presented by Zotina et al. (1999); more detailed data were provided by Degermendzhy and Gulati (2002). Lake Shunet is located (54°360 N and 90°200 S) in the northern part of Republic of Khakassia, Siberia. The maximum depth of Lake Shunet is 6.2 m. The surface area of the lake is 0.47 km2. The salinity of the water is 12.5 in the epilimnion and more than 40 ppt in the anoxic hypolimnion. The upper boundary of the monimolimnion is at a depth of 5 m. Hydrogen sulfide concentration in the Lake Shunet monimolimnion is usually about 450 mg L-1 (Rogozin et al. 2009), i.e. 15–20 times higher than in Lake Shira. The chemocline of the lake is characterized by a thin (5 cm) but dense layer of purple and green phototrophic bacteria (108 cells ml-1; Lunina et al. 2007) and a diverse community of microorganisms, comprising the ciliates Strombidium and Cyclidium spp. and mixotrophic flagellates Cryptomonas sp. (up to 105 cells ml-1; Khromechek et al. 2010). In both lakes, the dominant species of pelagic zooplankton are the calanoid copepod Arctodiaptomus salinus and several rotifer species (Anufrieva 2006; Zadereev and Tolomeev 2007). The vertical distribution and abundance of G. lacustris in the pelagic zone of two meromictic lakes, Shira and Shunet, was monitored with an underwater video recording system during stable thermal stratification (July–August) during 2005, 2007 and 2008 (dates are presented in Table 1).We used a KPC-600BH high-sensitivity (0.0003 lx) black-and-white CCD camera (KT&C, Korea), placed into a waterproof case. A wire frame was attached to the camera to fix the area of the picture (0.175 m2) within which the animals were counted. The camera was submerged from the surface of the lake down to the depth of 15 meters in Lake Shira or 5 meters in Lake Shunet at a speed of 0.1 m s-1. In each lake, we performed video recording at a roughly fixed station around noon time, in the pelagic region at the deepest sampling point. The vertical distribution of the gammarids was recorded taking between 5 and 10 videos on each monitoring date. The interval between videos was about several minutes. After each recording, we moved the boat several meters away and performed another video run. To examine potential diurnal changes in the vertical distribution of Gammarus in Lake Shira, we performed day (12:00, 5 July 2005) and night (00:00, 6 July 2005) recordings. Diel differences in
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Table 1 The abundance of Gammarus lacustris (ind m-2) in the pelagic deep stations of Lake Shira and Lake Shunet monitored with an underwater video camera Lake Shira
Lake Shunet
2005
2007
2008 2 July
5 July (day)
6 July (night)
27 July
278 ± 225
188 ± 146
(n = 10)
(n = 8)
Min
74
Max
606
Average abundance ± SE
2007
2008 08 August
6 July
24 July
28 July
115 ± 40 71 ± 69
107 ± 81
256 ± 143
423 ± 175 25 ± 18
(n = 7)
(n = 5)
(n = 5)
(n = 5)
(n = 10)
17
46
34
57
126
223
11
377
177
194
251
474
754
69
(n = 10)
SE standard error, n number of analyzed videos
distributions and numbers were compared using two-way analysis of variance (ANOVA) with daytime and depth as main effects. As amphipods were encountered in the water column at both night and day and their diurnal distribution was similar (see ‘‘Results’’ section), only day samples were taken at later dates and years. The abundance of Gammarus at different depths was determined from visual counting of animals from the video recordings each time. We first determined the average time period for which one animal was visible within the frame: 3.2 ± 0.5 s (n = 44). Based on this, we determined the abundance and the vertical distribution of G. lacustris from video recordings by counting the visible animals in each frame at 5-s intervals. The interval should exceed the average time period for which one animal is visible within the frame to avoid double counting of animals. We counted the number of animals in every 30–40 cm part of the water column. After every 5 s, the camera was moved 0.5 m deeper. Thus, every animal was counted just once. The average depth of Gammarus population in the water column was calculated as: d ¼
15 X i ni i¼0
n
;
where i is the depth, ni is the number of animals observed at the ith depth and n is the total number of observed animals. The depth of the thermocline was determined as the depth at which the temperature drop was maximal. The relationship of the thermocline depth with the average depth of Gammarus was assessed with linear regression.
To estimate the abundances of G. lacustris in the pelagic zone of Lake Shira, we also performed vertical hauls with the plankton net. This sample collection was conducted on 3 days in July 2008. We used plankton net with mesh size 160 lm and span diameter 0.45 m2. We sampled G. lacustris the same dates we performed video observations. Vertical hauls were taken from the depth 16 m (below the chemocline) to the surface. All animals from each sample were counted in the laboratory. Abundances estimated from vertical hauls were compared to those estimated from video records using linear regression. On the sampling dates of the animals in the two lakes, we also monitored the vertical profiles of temperature, salinity and oxygen concentration in the pelagic zones using an YSI 6600 submerged data sonde (YSI Corp., USA). Seston was sampled with a Ruttner-like 6 L sampler at 1-m intervals, from the surface to 15-m depth in Lake Shira and from surface to 5-m depth in Lake Shunet. The samples were prefiltered through 115-lm nylon mesh to remove larger zooplankton. For organic carbon and nitrogen measurements, seston was collected from the pre-filtered 500–1,000 ml water sub-samples by vacuum filtration onto precombusted GF/F filters (Whatman, USA). The samples for carbon and nitrogen were dried at ambient laboratory temperature overnight and stored in desiccator until analyses, which was performed with a Flash EA 1112 NC Soil/MAS 200 elemental analyzer (NEOLAB LLC, USA). The samples for analysis of particulate phosphorus, 300– 600-ml sub-samples were filtered onto membrane filters (pore size 0.45 lm). The background P content of the filters was measured earlier and subtracted from the obtained gross values for seston. The samples were oxidized using persulphate followed
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by color development using ammonium molybdate solution and measurement of extinction values using a spectrophotometer at 880 nm according to standard methods (Lenore et al. 1989). Differences in carbon, nitrogen and particulate phosphorus concentrations in seston with depth were assessed using ANOVA, followed by post hoc Fisher’s LSD tests. All statistical calculations during data analysis were performed in STATISTICA 6.0.
Results In July, Lake Shira is usually thermally stratified. During our observations, the depth of the thermocline increased during summer period. At the beginning of July, the thermocline was located at 4-m depth, while by the end of July the epilimnion expand and the thermocline sank to 6-7-m depth (Fig. 1). As is typical for this lake, the chemocline varied in its depth from 12.5 to 14 m. Lake Shunet was also thermally stratified during the sampling period (Fig. 2). The thermocline was located between 3.5 and 4 m, i.e. about one meter above the chemocline, located at a depth of 5 m.
Fig. 2 The abundances (individuals ± S.E.) of G. lacustris (open bars), temperature (t, °C), oxygen concentration (O2, mg L-1) and salinity (S, ppt) in the pelagic zone of Lake Shunet
Fig. 1 Day (open bars) and night (black bars) abundances (individuals ± S.E.) of G. lacustris, temperature (t, °C), dissolved oxygen concentration (O2, mg L-1) and salinity (ppt) in the pelagic zone of Lake Shira
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The distribution of Gammarus in the pelagic zone of both lakes during the stratification period, based on video recordings, was non-homogeneous. The animals in both Lake Shira (Fig. 1) and Lake Shunet (Fig. 2) exhibited their maxima in the thermocline. Pooled date of both lakes demonstrated that the average depth of Gammarus population strongly correlated with the position of the thermocline (Fig. 3) and this correlation between the two was statistically significant (P = 0.003). We did not find any significant differences between day- and night-time abundances of G. lacustris in the pelagic zone of Lake Shira, the maxima occurring in the metalimnion, with nocturnal peak situated 1 m below the daytime peaks. Factorial ANOVA demonstrated that the effect of daytime was insignificant (P = 0.18) while the effect of both depth (P \ 0.00001) and depth and daytime (P \ 0.00001) was highly significant. The abundance of G. lacustris in the pelagic zone of Lake Shira on 5 and 6 July 2005 was 278 ± 225 ind. m-2 during the daytime and 188 ± 146 ind. m-2, respectively. The records for other years were similar (Table 1). The correlation between the abundance of Gammarus in the pelagic zone of Lake Shira in July 2008 determined from video records and that determined using traditional vertical net hauls was positive and statistically significant (P = 0.0089; Fig. 4).
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Fig. 4 The correlation between the abundances of G. lacustris in the pelagic zone of Lake Shira in July 2008 determined using vertical net hauls and video recording. The dotted line is 1:1 line
The cumulative data on carbon, nitrogen and particulate phosphorus in the seston in pelagic zone of Lake Shira during summer stratification showed that the elemental concentrations (C, N, P) increased with increasing depth (Table 2). Post hoc comparisons demonstrated that the concentration of organic carbon in the metalimnion and the oxic and anoxic hypolimnion was slightly but significantly higher (P \ 0.05) than in the epilimnion. Nitrogen and particulate phosphorus concentrations did not significantly differ between the epilimnion and metalimnion concentrations. Both nitrogen and particulate phosphorus of seston in the oxic and anoxic hypolimnion significantly exceeded those in the epilimnion. In Lake Shunet, during summer stratification, the concentrations of all these elements in the seston of the oxic waters were uniform (Table 2). They increased dramatically at the depth of chemocline.
Discussion
Fig. 3 The correlation between the depth of the thermocline and the average depth of G. lacustris population in the pelagic zones of Lake Shira and Lake Shunet
Previous study on abundances of Gammarus in Lake Shira based on data that were collected in 1999 demonstrated that Gammarus lacustris was mostly found in the shore part of the waterbody from the water edge to the depth of 13.0 m (Yemelyanova et al. 2002). At 1.5–2.0 m depth, the densities of the amphipod was 278 ± 25 ind. m-2. At 5.0-m depth, the maximum density (414 ± 69.0 ind. m-2) was recorded. With increasing the depth from 12.0 to 22.0 m, the amphipod densities decreased from
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Table 2 The concentration (mg L-1 ± SE) of organic carbon (C), nitrogen (N) and particulate phosphorus (P) in seston of Lake Shira and Lake Shunet during summer stratification The water habitat
Lake Shira C, mg L-1
N, mg L-1
P, mg L-1
Epilimnion
1.870 ± 0.399
0.311 ± 0.066
0.022 ± 0.003
Metalimnion
2.428 ± 0.641
0.388 ± 0.082
0.034 ± 0.009
Oxic hypolimnion
2.364 ± 0.331
0.521 ± 0.158
0.042 ± 0.011
Anoxic hypolimnion
2.478 ± 0.454
0.508 ± 0.278
0.085 ± 0.025 P \ 0.00001
One-way ANOVA Overall P-value
P = 0.04
P = 0.049
Probabilities
Pepi-meta = 0.02
Pepi-meta = 0.38
Pepi-meta = 0.12
for post hoc
Pepi-hypo = 0.03
Pepi-hypo = 0.015
Pepi-hypo = 0.009
Fisher LSD test
Pepi-anoxy = 0.01
Pepi-anoxy = 0.025
Pepi-anoxy \ 0.0001
The depth interval, m
Lake Shunet C, mg L-1
N, mg L-1
P, mg L-1
0–4 5
1.869 ± 0.158 38.221 ± 16.018
0.264 ± 0.040 7.107 ± 3.310
0.026 ± 0.006 0.585 ± 0.353
t-test
P \ 0.0001
P \ 0.0001
P \ 0.0001
87 ± 12.0 to 43 ± 4.0 ind. m-2. Thus, the pelagic densities were 10 times lower than maximal densities in sub-littoral. We demonstrate that in pelagic part of the lake, abundances of Gammarus are comparable with that observed in littoral part. Abundances of Gammarus that were observed were highly variable throughout the season. Moreover, video recordings lasting several minutes demonstrate high variability of observed numbers (Table 1). Most probably, Gammarus exhibits swarming behavior, which requires many more observations to validate comparisons. Also we can propose that the abundances of Gammarus in the lake increased with time. During last 10 years, the water level of the lake increased and salinity in mixolimnion dropped (Rogozin et al. 2010). We can speculate that either because of salinity drop or lake elevation which increased the area of littoral or due to some other reasons abundances of gammarids in the lake increased; however, detailed whole lake sampling and comparison with previous data are required to confirm this hypothesis. Our results show that Gammarus is regularly present in the pelagic zone of two meromictic lakes, Shira and Shunet, during summer stratification. The gammarid exhibits peak densities in the thermocline on all sampling dates of all the study years. Thus, this
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type of vertical distribution is stable during summer stratification and typical for these lakes. Our data is not the first evidence of the vertical distribution of amphipods associated with the thermocline. Jesogammarus annandalei, an endemic amphipod in Lake Biwa, appears to be restricted to depths with a water temperature below 12°C. Amphipods performed diel vertical migrations; animals spend the day at the lake bottom and ascend to the pelagic zone at night. Gut fullness and gut contents of the migrating amphipods give clue to their feeding on plankton in the pelagic zone at night (Ishikawa and Urabe 2005). The use of high-frequency acoustic profiling demonstrates that at night in Lake Biwa, Jesogammarus annandalei tend to concentrate in the lower thermocline at the densities 15–20 ind. m-3 (Trevorrow and Tanaka 1997), which is comparable with our results. Melnik et al. (1993) observed a similar nocturnal vertical migration of amphipods Mucrohectopus brunickii in Lake Baikal: they found the peak densities in the upper thermocline. The authors attribute the migration of these amphipods to feed on zooplankton, abundant in the epi- and metalimnion. Seemingly, the animals choose that depth to minimize predation by adult fish, which are present in the epilimnion. There are other observations of Gammarus in open waters of several lakes (Wilhelm et al. 2000;
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Matafonov 2007). However, these studies lack data on vertical distribution structure of Gammarus and information on thermal stratification of water column. Wilhelm et al. (2000) reported that Gammarus is present in the water column of Snowflake Lake (Alberta, Canada). However, the distribution of Gammarus in Snowflake was not stratified. In Snowflake Lake, Gammarus was present in the water column only during the night. Matafonov (2007) studied the ecology of Gammarus lacustris in five lakes of the Trans-Baikal region (Russia), all of which are not meromictic. Among these lakes, G.lacustris was abundant in the pelagic zone of only Lake Bain-Cagan, which has a maximal depth of 6 m. In contrast with high densities in our lakes, the density of Gammarus in the pelagic zone of Lake Bain-Cagan was only one-seventh of that than in its littoral zone. It should be mentioned that previous studies on Lake Shira demonstrated close differences between littoral and pelagic abundances of Gammarus (Yemelyanova et al. 2002). Thus, pelagic occurrence of G. lacustris is not common. Most probably, specific environmental conditions can lead to such an adaptation. The vertical distribution of Gammarus apparently reflects its physiological or ecological preferences or both. There are two important trophic factors, predation pressure and food availability that can influence the vertical distribution of species. The absence of fish, let alone predatory fish, and other predators in the pelagic zones of these lakes is an important factor that allows Gammarus to stay in open waters of Lake Shira and Lake Shunet. The source of food for Gammarus in pelagic zone of studies lakes is not investigated yet. Examination of the gut contents of Gammarus lacustris from the littoral zone of Lake Shira performed in a previous study (Gladyshev et al. 2000) shows that Gammarus primarily ingests seston. Other studies demonstrated that detritus is the major item in guts of juveniles of G. lacustris, while contribution of detritus in guts of adults significantly decreased where proportion of animal food significantly increased (Berezina 2007). Analysis of the fatty acid composition of gut contents and bodies of Gammarus collected near the shore and in the pelagic zone of Lake Shira did not reveal any compositional difference in fatty acids between them (Zadereev et al. unpublished). Thus, we can assume that in pelagic Gammarus also feeds on seston. This
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assumption is also confirmed by our previous experiments with mesocosms which demonstrated that Gammarus can survive for a long period in Lake Shira water with natural seston particles (Tolomeyev et al. 2006). The thermocline can act as a barrier for the settling seston and detritus (e.g., Kufel and Kalinowska 1997). In Lake Shira, the total amount of carbon, nitrogen and phosphorus in seston in the metalimnion was slightly higher than in the epilimnion. However, the difference was significant only for carbon. The concentration of seston was even higher in the hypolimnion and the monimolimnion. Nevertheless, Gammarus preferred to stay in the metalimnion. In Lake Shunet, the total amount of carbon, nitrogen and phosphorus in seston in the upper 4 m was distributed uniformly. The concentration of all nutrients dramatically (20-fold) increased at the chemocline. However, again the peak abundance of Gammarus was associated with the thermocline rather than with the chemocline—thus away from depth where seston maximum occurred. Dissolved oxygen and temperature can be factors that responsible for the high abundance of G. lacustris in the thermocline. Lake Shira has a deep chlorophyll maximum (Gaevsky et al. 2002). The maximum of oxygen concentration in Lake Shira during summer stratification is usually observed above the maximum of chlorophyll in the metalimnion. It is well known that Gammarus prefers cold, oxygen-rich waters (Khmeleva 1988). It seems that Gammarus chooses a location with an optimal combination of several factors: optimal temperature, a high level of dissolved oxygen and high seston concentration. Another explanation for the peak densities of Gammarus in the metalimnia of the studied lakes is based on the profiles of temperature and salinity, and hence, water density. G. lacustris may lead a pelagic existence because it achieves neutral buoyancy in cold saline waters. In both Lake Shira and Lake Shunet, salinity increases as the temperature decreases with increasing depth. The decrease in temperature and increase in salinity lead to an increase in water density (e.g., in the thermocline of Lake Shira, the water density in the thermocline is increased by 0.4%). The water below the chemocline is anoxic, which is lethal for Gammarus. Thus, the metalimnion is habitat with the highest water density,
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which allows predominantly benthic organisms to be pelagic as they can invest minimal energy in maintaining their place in the water column. To confirm this hypothesis, the buoyancy of amphipods should be measured in waters of different densities. Even though we assume that the combination of physicochemical and biological factors forces Gammarus to occupy the metalimnion, it is not clear why benthic animals should stay in open waters. Lakes Shira and Shunet are meromictic. Hence, in the pelagic zone, the bottom habitat is not available for Gammarus. The abundance of Gammarus in the pelagic zone of Lake Shira reaches 400–600 ind. m-2, which is comparable with the abundance of Gammarus in the littoral part of the lake (Yemelyanova et al. 2002). If we assume that Gammarus cannot live throughout the year in open water, the animals should perform long-distance horizontal migrations to find a suitable littoral bottom habitat. The reason why they perform such migrations is not known. We also should not forget about the long period when shallower littoral waters are the first to freeze and keep frozen. It could also force the animals to move to open waters and survive winter in the deeper layers. We conclude that widely distributed in lakes G.lacustris demonstrated very high adaptive potential. Under specific conditions, they are able to switch to pelagic life style which is unexpected from predominantly benthic animals. To demonstrate the phenomenon is the first step. The next step is to explain what external or internal factors forced animals to occupy this niche. Future research should focus on patterns of horizontal migrations, physiological or ecological preferences and feeding ranges of Gammarus in the pelagic zone in order to gain insight into its complex population dynamics and role in the functioning of the ecosystem. Acknowledgments The work was supported by Project N2004 0.47.011.2004.030 (the Russian Foundation for Basic Research and the Netherlands Organization for Scientific Research), grant No. PG07-002-1 of the CRDF and the Ministry of Education and Sciences of Russian Federation; grants of Russian Foundation for Basic Research (RFBR) Nos. 08-04-01232 and 08-04-00928. The work was partially supported by Integration project of SB RAS No. 95. We are grateful to the three anonymous reviewers for their valuable advice to improve an earlier version of the manuscript. Special thanks to E. Krasova for linguistic improvements and Dr. Ramesh Gulati for valuable corrections.
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