Plant Pigments in Bottom Sediment Cores as Indicators of the Trophic State in Large Shallow Lakes Vozhe and Lacha (Russia)

The first data on the content of plant pigments is presented for the cores of bottom sediments sampled in large shallow lakes Vozhe and Lacha located in the upper reaches of the Onega River. In the 1-m core of olive silts, the total concentration of chlorophyll a and pheopigments varied within 35–236 (94.2 ± 3.3) in Lake Vozhe and 58–118 (83.8 ± 1.3) μg/g dry sediment in Lake Lacha. The degree of chlorophyll destruction in the cores from Lake Lacha (98.7 ± 0.2%) was higher than in Lake Vozhe (85.2 ± 0.7%). Considering the average long-term sedimentation rate of 0.2 and 0.4 mm/year in Lakes Vozhe and Lacha, respectively, the annual vertical flux of chlorophyll a and pheopigments is 4.0 and 6.2 mg/(m2 · year) for the last 2500 years, respectively. Nowadays, the average annual rate of pigment accumulation is almost the same in the lakes (5.6 and 5.3 mg/(m2 · year)). Over the period under consideration until now, different patterns of long-term dynamics of pigment accumulation in the studied lakes have been revealed; in particular, there is a positive trend in Lake Vozhe and a negative trend in Lake Lacha.


INTRODUCTION
The eutrophication of fresh and marine waters is a global problem of the modern era of increasing anthropogenic influence and significant climatic fluctuations (Smith, 2003;Maheaux et al., 2016;Tsugeki et al., 2017;Deng et al., 2018aDeng et al., , 2018bHuo et al., 2018;Yao et al., 2018;Zhao and Fu, 2019). It is important to know and predict the trophic state of diverse aquatic ecosystems as the basis for their structure and functioning. The ecological state of aquatic ecosystems largely depends on the ability of plant communities to create primary organic matter (OM) using solar energy (Vinberg, 1960;Rossolimo, 1977;Alimov, 2000;Deng et al., 2018aDeng et al., , 2018b. Plant pigments are considered integral indicators of the trophic state; their concentrations reflect almost all stages of the synthesis and transformation of OM, from primary to final production (Swain, 1985;Leavitt, 1993;Sigareva, 2012). In hydroecology, data on the spatiotem-poral distribution of pigments in bottom sediments (BS's) are widely used (Sigareva et al., 2021). According to the vertical profile of pigments in sediment cores, the history of reservoir productivity and, accordingly, the dynamics of the trophic state of its ecosystem are restored (Möller and Scharf, 1986;Szymczak-Żyła and Kowalewska, 2009;Tsugeki et al., 2017). Particular difficulties arise when studying ecosystems of shallow flowing water bodies, which are affected most strongly by abiotic factors and where the temporal (layer-by-layer) accumulation of BS's is not expressed.
Lakes Vozhe and Lacha form a system of flowing lakes connected by the Svid' River (Gidrologiya …, 1979). The lakes are in the upper reaches of the largest river of northwestern Russia, the Onega River, flowing through Vologda and Arkhangelsk oblasts (regions). The lakes are far from centers of economic activity and are used for recreation and amateur fishing. The area of Lake Vozhe is 418 km 2 and Lake Lacha is 345 km 2 ; the average depth is 1.4 and 1.6 m and the normal retaining level is 122 and 118 m of Baltic System, respectively. The catchment area is formed by deposits of glacial origin. Swampiness is 15%, forest cover is 77%, and agricultural development is ~8% of the catchment area. The conditional water exchange coefficient in Lake Vozhe is 3.5 year -1 and 7.4 year -1 in Lake Lacha. Intense winds are the main factor of hydrodynamic activity; they lead to a change in the direction of currents and affect the functioning of the ecosystem of lakes. The surface current flow in Lake Vozhe reaches 17 cm/s and 13 cm/s in Lake Lacha. From 1973 to 2015, overgrowth by higher aquatic vegetation in Lake Vozhe increased from 18.3 to 26% and, in Lake Lacha, from 45 to 70% (Gidrobiologiya …, 1978;Otchet …, 2015).
In Lake Vozhe, the processes of suspended matter transfer predominate; in Lake Lacha, sedimentation processes prevail. The main area of the bottom in Lake Vozhe is occupied by coarse-grained sediments of various types (60%); in Lake Lacha it is occupied by olive silts (88%) (Gidrologiya …, 1979;Zakonnov and Chuiko, 2019). The greatest thickness of deposits in the lakes is noted in the depressions of the bed, in particular, in the glacial karst hollow in the southern part of Lake Vozhe and in a series of karst funnels near the southwestern and northeastern coast of Lake Lacha. The rate of silt accumulation in Lake Vozhe is 0.1-0.2 mm/year; in Lake Lacha, it is 0.2-0.4 mm/year.
This study aims to identify long-term trends in the productivity of large shallow flowing lakes Vozhe and Lacha (northwestern Russia), characterized by a flat bottom, an intense hydrodynamic regime, and high overgrowth (while considering the vertical distribution of plant pigments in sediment cores).

MATERIALS AND METHODS
Cores (1 m in thickness) were obtained in July 2015 from karst funnels with a tubular rod bottom grab invented by F.D. Mordukhai-Boltovskoy at 4-m-deep stations in Lake Vozhe (60°59′6.13″ N, 39°07′7.51″ E) and 3-m deep ones in Lake Lacha (61°32.8′6.09″ N, 38°7.38′18.3″ E). The cores were cut into 1-cm layers. Chlorophyll a (Chl) and pheopigments (Pheo) concentrations were determined in wet samples by spectrophotometry on a Lambda 25 spectrophotometer (PerkinElmer, United States) according to standard methods (Lorenzen, 1967;Sigareva, 2012). The pigment concentration was calculated in different units: per dry sediment (μg/g), per area of wet sediment of natural moisture at a 1-mm layer (mg/(m 2 · mm)), and per OM of bottom sediments (mg/g OM). The indexes E 480 /E 665 and E 480 /1.7E 665a were used as indicators of the ratio of the concentration of carotenoids and Chl. The natural water content was determined by drying the samples at 60°С, the OM content was determined by the weight loss of dry sediment during calcination at 600°С, and the air-dry volumetric mass was determined by a method developed earlier (Sigareva et al., 2019). The average annual rate of pigment accumulation was calculated for 50-year periods based on the content of Chl + Pheo in 1-cm layers of wet sediment of Lake Vozhe and 2-cm layers of Lake Lacha and considering the sedimentation rate in Lake Vozhe to be 0.2 mm/year and, in Lake Lacha, 0.4 mm/year (Gidrologiya …, 1979).
The average content of plant pigments was determined for the entire thickness of the cores, as well as for the upper (0-10 cm) and lower (11-100 cm) parts. In addition, the coefficients of variation and determination coefficients of Chl + Pheo content with water content, air-dry volumetric mass, and OM content in dry sediment were calculated. The significance of differences was assessed by Student's t-test.

RESULTS
The core from Lake Vozhe is olive fine silt underlaid by blue-white clay at a depth of 90-100 cm; the core from Lake Lacha is olive silt without a marking layer. Considering the silt accumulation rate to be 0.2 mm/year in Lake Vozhe and 0.4 mm/year in Lake Lacha, the approximate age of silts in cores differs almost twofold, 4450 and 2500 years, respectively. The age of 1-cm layers in the Lake Vozhe core is estimated as ~50 years and, in Lake Lacha, ~25 years.
The upper layers of the cores (0-15 cm) were heavily watered; the underlying deposits were characterized by a compacted consistency. The water content of silt in Lake Vozhe was in the range of 65.8-89.1% and the air-dry volumetric mass was 0.12-0.44 g/cm 3 ; in Lake Lacha, they were 76.1-88.0% and 0.13-0.28 g/cm 3 , respectively. In the lower part of the core from Lake Vozhe, in white-blue clay deposits, the water content decreased to 37-46%, while the volumetric mass increased to 0.76-1.06 g/cm 3 . The average values of water-physical indicators of olive silt did not differ significantly in either lake (Table 1).
The Chl + Pheo content in the Lake Vozhe core varied from 35.1 to 236 (94.2 ± 3.3) and, in Lake Lacha, from 58.3 to 119 (83.8 ± 1.3) μg/g dry sediment (Figs. 1, 2). The coefficient of variation of Chl + Pheo concentrations in the core from Lake Vozhe significantly exceeded that from Lake Lacha. Other indicators of the content of sedimentary pigments were comparable for both lakes or slightly higher in Lake Vozhe (Table 1).
In the core from Lake Vozhe, vertical profile of Chl + Pheo content, expressed in different units, was characterized by an increase in the index from the lower layers to the upper ones ( Fig. 1) and, in Lake Lacha, by some decrease (Fig. 2). At the same time, in both lakes, the OM content dynamics was not clearly expressed and no differences were found (Figs. 1d,2d). Along the core, the OM contribution was most often the same, with a minimum content noted in the lower part of the core from Lake Vozhe. The pigment concentration was most variable in the upper 10 cm of the core from Lake Vozhe. In the upper (0-10 cm) and lower (11-100 cm) parts of cores in Lake Vozhe, average concentrations of Chl + Pheo, calculated for dry sediment, OM, and wet sediment of natural moisture, exceeded the corresponding values in Lake Lacha ( Table 2).
The degree of Chl degrading was characterized by the highest values in Lake Lacha, reaching 99.8% with minimal vertical variability (C v = 2%). In Lake Vozhe, the contribution of pheopigments was maximum in the underlying layer (97.3%) with an insignificant content of Chl + Pheo (1.3 μg/g dry sediment). The carotenoid-to-Chl ratio in the cores from the studied lakes corresponded to the values known for other water bodies. In Lake Vozhe, the E 480 /E 665 ratio varied from 1.48 to 3.23. The E 480 /1.7E 665a ratio, reflecting the carotenoid-to-Chl ratio considering Pheo content, varied from 0.99 to 2.01. In Lake Lacha, the first index varied from 2.82 to 4.30 and the second one from 1.13 to 2.54. Average index values in the core from Lake Vozhe were noticeably lower than those in the core from Lake Lacha (Table 1). Differences in the degree of pigment degrading remained when comparing the upper and lower parts of the cores from both lakes; in particular, the relative content of pheopigments was lower in both parts of the core from Lake Vozhe when compared to those from Lake Lacha ( Table 2).
The Chl + Pheo content in the core from Lake Vozhe corresponded to the typological indicators of sediments, i.e., the determination coefficient (R 2 ) between pigments and water content was 0.67, between pigments and volumetric mass 0.72, and between pigments and OM content 0.52. However, no relationship between pigment and typological charac-teristics was found in the Lake Lacha core, which was confirmed by a slight variability in the values.
In Lake Vozhe, the most intense increase in the Chl + Pheo content per dry sediment was registered over the past 500 years (upper 10-cm layer) and 4000 year ago (80-100 cm) (Fig. 1). On the contrary, in Lake Lacha, the pigment concentration dynamics was more chaotic, with a noticeable general trend of decreasing Chl + Pheo concentration to the present time from the beginning of the period under consideration (2500 years ago).
The pigment accumulation rate (Chl + Pheo) was uneven in the average annual sediment layer along the core: on average, it was 3.9 mg/(m 2 year) in Lake Vozhe and 6.2 mg/(m 2 year) in Lake Lacha. However, in the upper 5-cm layer, the average annual pigment accumulation rates were nearly the same, 5.6 mg/(m 2 year) in Lake Vozhe and 5.3 mg/(m 2 year) in Lake Lacha. In deeper layers, the annual pigment accumulation rate was noticeably higher in Lake Lacha than in Lake Vozhe (Fig. 3a). In general, the average annual content of Chl + Pheo tended to increase up to the present in Lake Vozhe; the opposite pattern was observed in Lake Lacha. A significant negative correlation coefficient (-0.49) was noted between the annual pigment accumulation rates in the cores from lakes Vozhe and Lacha, reflecting different directions of changes in the long-term dynamics of production processes. It is noteworthy that general long-term dynamics of the average annual accumulation of pigments in both lakes has been characterized by increased values in recent years (~350 years), but no general trend over the entire period under consideration has been traced (Fig. 3b). The total pigment accumulation rate for the two lakes over the period under consideration varied slightly from 8 to 12 mg/(m 2 · year) (C v = 9.5%) along the entire core.

DISCUSSION
Plant pigments, first and foremost, Chl, are the most important in the study of eutrophication of aquatic ecosystems, since the fundamental trophodynamic indicator, the increase in the rate of primary production of OM due to biogenic elements, is difficult to assess (Sigareva, 2012). In addition to the basic indicators of eutrophication (nutrients, Chl, and water transparency), much attention is currently paid to the factors of productivity associated with climate warming. First and foremost, these are an increase in the intensity of ultraviolet radiation and a decrease in wind activity, as well as the dynamics of the oxygen regime in the reservoir, water mass exchange, nutrients, and suspended matter (Martynova, 2008;Maheaux et al., 2016;Andersen et al., 2017;Deng et al., 2018aDeng et al., , 2018b.  The depletion of oxygen in the near-bottom water layer and BS leads to an increase in the solubility of phosphorus compounds and an increase in the internal nutrient load, which stimulates eutrophication (Martynova, 2008;Yang et al., 2020). By creating primary OM, ecosystems may respond differently to abiotic conditions (Rossolimo, 1977;Alimov, 2000;Kitaev, 2007). A decrease in the water body depth due to the accumulation of bottom sediments in the process of ecosystem evolution is considered evidence of eutrophication (Datsenko, 2007). However, in some shallow lakes, intense hydrodynamic activity prevents the sedimentation of suspended matter and the formation of interannual layering of sediments; therefore, eutrophication in such ecosystems may be tracked by average long-term trends in trophic indicators related to a number of years. Such reservoirs includes Lake Vozhe. A flat bottom and intense wind activity contribute to trans-sedimentation, i.e., the predominance of suspension removal over sedimentation. Signs of eutrophication in this lake have been noted earlier during studies of ichthyofauna as a part of the lake community (Bolotova et al., 1996). In our study, the eutrophi-cation of Lake Vozhe has been identified by studying the dynamics of plant pigments in a single core. The vertical distribution of Chl + Pheo in the core is characterized by the most rapid changes during the last 500 years and a generally positive trend in the accumulation of pigments over the entire considered period of ~4500 years. The nature of the pigment dynamics in the 1-m core from Lake Vozhe is consistent with that reported for different types of water bodies, where cores of similar length have been analyzed. An analysis of the cores in a number of water bodies (mesotrophic Lake Pleshcheyevo, Lake Naroch, and Rybinsk Reservoir and hypertrophic Lake Nero) evidences that the vertical distribution of plant pigments reflects a widespread increase in the rate of eutrophication at the present stage of evolution (Sigareva, 2012;Guseva and Ivanov, 2018;Smol'skaya and Zhukova, 2019).
A completely different pattern is noted for Lake Lacha, which receives the waters of Lake Vozhe through the Svid' River. Lake Lacha is characterized by the predominance of sedimentation over the removal of suspended matter. However, the long-term dynamics of pigments in the core is not typical: in the uppermost part of the core (≤5 cm), only a slight increase in the content of Chl + Pheo is observed; concentrations of pigments decrease during the entire period under consideration (~2500 years) to date. The vertical variability of biotic parameters depends on the type of sediment (Sigareva, 2012;Yin et al., 2016). However, this factor could not be a reason for the observed differences in the trends of sedimentary pigments, since olive silt is the only type of sediment in lake cores. If we consider Lake Lacha part of a single water system including Lake Vozhe, then a decrease in the concentration of pigments in the upper part of the column in the first reservoir along with an increase of this indicator in the second one may be considered the result of ecosystem interaction. It is noteworthy that the average concentrations of pigments (in terms of dry sediment) in the cores of the same type of sediment in both lakes are similar and refer to a eutrophic state (Möller and Scharf, 1986). However, according to the average annual accumulation rate of Chl + Pheo in BS, the trophic state of Lake Lacha is higher than that of Lake Vozhe throughout almost the entire period under study. In recent centuries, the trophic state of both lakes has become similar. An analysis of the reasons for differences in lakes regarding the nature of vertical distribution of plant pigments in cores, and, consequently, the rate of eutrophication, may be based, first and foremost, on ideas about the role of a watershed area in shaping the productivity of water bodies. Bottom sediments are not only a product of the interaction between abiotic conditions and the biota of a water body, but also a product of the influence of the watershed area on the aquatic ecosystem (Vorontsov and Spasskaya, 1984;Martynova, 2007Martynova, , 2008. According to (Gidrologiya …, 1979), the catchment area of Lake Lacha (12130 km 2 ), as well as the water exchange (7.4 year -1 ), is almost twice as large as Lake Vozhe (5870 km 2 and 3.5 year -1 , respectively). Therefore, one may expect that intensive water exchange contributes to the rapid water turnover in Lake Lacha due to the large number of tributaries that create a high external nutrient load. At the same time, the increased overgrowth of Lake Lacha by macrophytes limits hydrodynamic activity and creates conditions for oxygen stratification. Considering pigment concentration in terms of dry sediment (~100 μg/g), both lakes were similar for a long time; the concentration of pigments in Lake Vozhe is almost twice as high as that in Lake Lacha only in the modern period. The contents of pigments per 1 m 2 and per OM also change similarly. At the same time, both lakes are characterized by similar annual accumulation rates of plant pigments in recent years.
The enrichment of waters with mineral nutrients due to deforestation, mole rafting in the 19th century, and the regulation of water flow by a low-pressure dam on the Svid' River are anthropogenic factors that might cause large-scale changes in the ecosystems of lakes Vozhe and Lacha at the present stage of evolution (Zakonnov and Chuiko, 2019). The results suggest that the productivity of Lake Vozhe has increased, while that of Lake Lacha has decreased.
According to previous studies, lakes Vozhe and Lacha differed in trophic state. Lake Vozhe was assessed as mesotrophic with signs of eutrophication according to the characteristics of the structure of the fish population, i.e., a decrease in species diversity and an increase in the dominance of short-cycle species (Bolotova et al., 1996). Lake Lacha was characterized as weakly eutrophic in terms of the development of phytoplankton and higher aquatic vegetation (Katanskaya and Letanskaya, 1986). In regard to the parameters of zoobenthos (Gidrobiologiya …, 1978;Ivicheva and Filonenko, 2015) and zooplankton (Novoselov et al., 2017), Lake Lacha was considered eutrophic. The data of our study give an idea of the dynamics of the trophic state of the Vozhe-Lacha lake system.

CONCLUSIONS
The nature of long-term dynamics of sedimentary pigments in two large shallow communicating lakes, forming a single water system, is revealed. Despite the similarity of lakes by geomorphological indicators and location in the same climatic zone, trends in changes in all indicators of the content of plant pigments along the core are asynchronous. To date, the concentration of Chl + Pheo increases in Lake Vozhe and decreases in Lake Lacha. Due to the cascade arrangement of the studied reservoirs, the productivity of Lake Vozhe located upstream is lower in terms of the average pigment accumulation rate in the core compared to Lake Lacha located downstream. These results deepen the understanding of eutrophication processes in the northern pristine lake ecosystems unaffected by anthropogenic pollution.

FUNDING
This study was performed in accordance with State Tasks nos. 121051100099-5 and 121051100104-6.

COMPLIANCE WITH ETHICAL STANDARDS
Conflict of interest. The authors declare that they have no conflicts of interest.
Statement on the welfare of animals. This article does not contain any studies involving animals or human participants performed by any of the authors.

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