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Project titleBiotic transfer of substances from water to land from small water bodies of the European forest-steppe

Research area 04 - BIOLOGY AND LIFE SCIENCES, 04-103 - Hydrobiology and ichthyology

Keywordsaquatic ecosystems, terrestrial ecosystems, transfer of matter, forest-steppe, land/inland-water ecotones, amphibionts, polyunsaturated fatty acids

Annotation
The relevance of research is associated with the ever-increasing natural and anthropogenic impact on aquatic and riparian ecosystems. Small continental water bodies, which were underestimated by researchers for a long time, turned out to be especially vulnerable, although recently their great importance for biodiversity and geochemical cycles has been proven (Downing, 2010; Céréghino et al., 2014; Bolpagni et al., 2019). Recently, the importance of studies of both the structure and function of these aquatic ecosystems themselves and their interactions with terrestrial ecosystems has become obvious. At the same time, it turned out to be extremely important to obtain new knowledge not only on the exchange of matter and energy between ecosystems due to abiotic factors (for example, diffuse runoff, channel processes, floods, drying up of water bodies), but also on the role of biota in this exchange. In particular, the processes of transfer of organic substances produced in the aquatic environment to terrestrial ecosystems have not been sufficiently studied. The novelty of this work lies in planning the assessment of not only the total volumes of organic matter produced by aquatic organisms and transferred to land but also their qualitative composition. Particular attention will be paid to those substances that are produced by living organisms in one of the environments and are in short supply in the other. One of the groups of such substances is polyunsaturated fatty acids (PUFA), which are essential for many terrestrial animals, but are effectively formed mainly by phytoplankton organisms (Gladyshev et al., 2009; Gladyshev, Sushchik, 2019). Among the PUFAs necessary for the normal functioning of the cardiovascular system and other physiological and biochemical processes of terrestrial vertebrates, eicosapentaenoic and docosahexaenoic acids are especially important. Studies of the content of these PUFAs in aquatic, amphibiotic, and terrestrial organisms make it possible not only to establish the nature of the transfer of substances between different ecosystems but also to understand the mechanisms of the functioning of their trophic webs, using these compounds as biochemical marks. In the slightly watered natural areas of the European forest-steppe, water bodies are usually represented by only small objects, which makes them key sources of water subsidies for terrestrial ecosystems. One of the most common types of small water bodies are floodplain lakes and oxbows. In modern conditions, due to changes in the water regime of rivers and hydroelectric construction, floodplain ecosystems lose their connection with the river and degrade (Tockner, Stanford, 2002; Nilsson et al., 2005). In the forest-steppe zone of European Russia, a decrease in the level of spring floods was noted (Frolova et al., 2015; Dmitrieva, 2020), which leads to shallowing and plant overgrowing of oxbow lakes. Such changes in habitats directly affect food webs and the transfer of matter from the aquatic environment to terrestrial ecosystems (Schindler and Smits, 2017). At the same time, compared to large objects, small reservoirs export PUFA in a larger volume per unit area (Fritz et al., 2019). In addition, small water bodies, including temporary and drying up, are distinguished by a very close relationship with the surrounding terrestrial ecosystems, therefore, they can serve as a qualitative model for studying the flow of matter through transition zones (“land-inland water ecotones”). The interaction of aquatic and terrestrial ecosystems is one of the priority problems of modern ecological science. The border areas of ecosystems (ecotones) actually function as membranes that regulate the flow of matter and energy between adjacent spots of the resource. In such transit zones, important interactions of biological objects of all levels take place, and high rates of biodiversity and biological productivity are often observed (Dgebuadze, Gladyshev, 2016). The relevance of the topic is also closely related to the need for research on amphibiotic animals: insects, amphibians, reptiles, and mammals, the role of which is the transfer of substances to land is not well studied. For many of these organisms, due to global changes, there is a decrease in diversity and abundance. In particular, in recent decades, in many regions of the Earth, a decrease in the abundance and diversity of amphibians has been noted (Campbell Grant et al., 2020), which necessitates obtaining new knowledge on their trophology, distribution, and production. Recently, the activity of the amphibiotic species, the Eurasian beaver (Castor fiber), has also been of great importance for the transfer of substances for the water bodies of the forest-steppe zone. The construction activity of beavers leads to the emergence of new types of water bodies (beaver ponds), a change in the length of the coastline, which actually contributes to the restructuring of existing ecotones and the creation of new ones (Zavyalov, 2016). Under the influence of these changes, both aquatic and riparian ecosystems are significantly rebuilt.

Expected results
As a result of the project implementation, data on feeding, growth, abundance, biomass, and production of mass aquatic and amphibiotic animals of benthos and nekton in small continental water bodies of the forest-steppe zone will be obtained and will be revealed their role in the transfer of organic matter from aquatic to terrestrial ecosystems. New data will be obtained on the qualitative composition of matter in the trophic webs of water bodies, in particular, evidence on the content of polyunsaturated fatty acids in the biomass of various organisms. In addition, a quantitative assessment of the biotic transfer of these lipids by amphibiotic insects, amphibians, and reptiles from aquatic to terrestrial ecosystems will be carried out. This knowledge is of great practical importance in the future, in view of the importance of PUFA for vertebrates (including humans), which are not able to efficiently synthesize these substances essential for their life. Comparison of the data obtained from water bodies of different genesis will make it possible to establish the role of the activity of the key species, the Eurasian beaver, for the flows of matter and energy in aquatic ecosystems of small water bodies of the forest-steppe. Such assessments are important in connection with climatic changes, and the observed degradation of natural reservoirs and watercourses.

Annotation of the results obtained in 2023
The role of various abiotic factors (depth, water regime, plant cover, water temperature, pH, dissolved oxygen content in water) affecting various aquatic organisms in small water bodies of the forest-steppe zone of Russia (beaver ponds, floodplain water bodies, river pools) was analyzed and biotopic differences in their distribution were revealed. New data on seasonal and interannual dynamics of these abiotic characteristics in different types of water bodies was obtained. The food preferences of a model fish species Leucaspius delineates in different habitats were determined using data obtained by the traditional method (by gut content). In terms of frequency of occurrence of feeding components, terrestrial Homoptera (29.6%), planktonic crustaceans (29.5%) and larvae of Diptera (26.6%) were predominant. At the same time, food preferences differed in different water bodies. In the river, crustaceans (39.3%) were most often found in the guts, while in beaver ponds – Diptera (61.5%). Thus, our results revealed that after the river is dammed by beavers, the feeding spectrum of L. delineates changes, they switch from benthic food to zooplankton, which in beaver ponds is characterized by greater abundance and biomass. In addition, data were obtained on PUFA content in the biomass of this fish. The total fatty acid content was 22.1±6.44 mg/g wet weight, EPA concentration was 2.2±0.59 mg/g wet weight, DHA concentration was 2.1±0.30 mg/g wet weight, which is rather high for fish of the order Cyrpiniformes. A quantitative assessment of the biotic transfer from aquatic to terrestrial ecosystems was carried out using insects, amphibians and reptiles as examples. The average value of substance flux (wet weight) carried from water to land by metamorphs of the moor frog (Rana arvalis) was 0.19 g/m2 per year. The absolute abundance of the grass snakes Natrix natrix in the floodplain system and the sex and age structure of the population were determined using the recapture method. The biomass of adult snakes was estimated at 657 g/ha, the growth rate of snakes was 260 g/ha per year. Based on the comparison of species with short (moor frog) and long (Pallas's spadefoot toad) development, the role of duration of metamorphosis for PUFA accumulation by amphibian larvae was evaluated. The differences between the samples of these species were largely due to differences in the levels of 18:4n-3 FA and ∑16PUFA (the sum of 16-atom PUFAs) (markers of microalgae), on the one hand, and 24:1 (markers of higher plants) and C18-20 monounsaturated FAs (de novo synthesis products in animals), on the other hand. In addition, in the second dimension, significant differences were found between R. arvalis tadpoles, on the one hand, and P. vespertinus tadpoles and metamorps, on the other hand, which were mostly due to the differences in the levels of 12:0 and 18:4n-3 FAs in their biomass. The 18:4n-3 FA, which was present in relatively high amounts in P. vespertinus tadpoles and metamorphs and was absent in grass snakes, is a marker of cryptophyte and chrysophyte algae. The total content of EPA + DHA in metamorps of both species and grass snakes was significantly higher than in tadpoles, which indicates the accumulation of these essential PUFAs in the biomass of amphibians during metamorphosis, as well as in the biomass of grass snakes as top-level consumers in relation to amphibians. The use of fatty acids as biomarkers (higher levels of the essential linoleic acid 18:2n-6) showed that R. arvalis metamorps have a higher proportion of terrestrial food in their diet than P. vespertinus metamorps. Differences in markers may be associated with the development of these two species, which differs in timing and duration. The first data on the influence of the key-stone species, the Eurasian beaver Castor fiber, on substance flows within floodplain water bodies were obtained. Microhabitats (channels) created by beavers differed from unaffected parts of water bodies by greater depth, less overgrowth and higher dissolved oxygen levels. This influenced amphibian metamorphosis as it led to redistribution of tadpoles and affected their development rates.

Publications

1. Bashinskiy I.W., Dgebuadze Yu.Yu., Sushchik N.N., Osipov V.V., Gladyshev M.I. Spadefoot Pelobates vespertinus (Amphibia, Pelobatidae) as a transmitter of fatty acids from water to land in a forest-steppe floodplain Science of The Total Environment, V. 877, 162819 (year - 2023) https://doi.org/10.1016/j.scitotenv.2023.162819

2. Dgebuadze Yu.Yu., Neymark L.A., Bashinskiy I.W., Sushchik N.N., Rudchenko A.E., Gladyshev M.I. Роль обыкновенного ужа Natrix natrix (Reptilia, Colubridae) в переносе полиненасыщенных жирных кислот из водных экосистем на сушу Доклады Российской академии наук. Науки о жизни, Т. 513. С. 83–87 (year - 2023) https://doi.org/10.31857/S2686738923700440

3. Silina A.E., Sushchik N.N., Gladyshev M.I., Kurina E.M., Kolmakova A.A., Seleznev D.G. Вылет амфибиотических насекомых из старого бобрового пруда в долине Верхнего Хопра в лесостепной зоне Сибирский экологический журнал, № 6. С. 872–892 (year - 2023) https://doi.org/10.15372/SEJ20230612

4. - Лягушки оказались полезным источником полиненасыщенных жирных кислот Наука в Сибири, - (year - )

Annotation of the results obtained in 2022
The study of biotic transfer of substances in the ecosystems of small water bodies in the upper reaches of the Khoper River on the territory of the Privolzhskaya Lesostep nature reserve (Kolyshleysky district, Penza Oblast) and its vicinities was carried out. To analyze the quantitative composition of substance in trophic fluxes of water bodies, we obtained data on the biomass and production of fish and amphibian larvae in different habitats. At the first stage, the structure of the communities of anamniotes in terms of abundance was assessed. The beaver ponds were dominated by the sunbleack Leucaspius delineatus (40%), tadpoles of the marsh frog Pelophylax ridibundus (34%), and larvae of the common newt Lissotriton vulgaris (20%). In the control habitats - riverbed pools - also sunbleack (75%) and loach Barbatula barbatula (19%) were dominated, and amphibian larvae were not found. In floodplain water bodies tadpoles of spadefoot Pelobates vespertinus (74%) and larvae of common newt (13%) were dominated. Fishes were practically absent, and only one species – goldfish Carassius carassius (2%) was found. The mean abundance of sunbleack was 20.4 ind/m2 in stream pools, and 10.4 ind./m2 in beaver ponds. Average biomass was 4.1 g/m2 in stream habitats, and 3.9 g/m2 in ponds. The sunbleack production in the studied water bodies reached 0.22 g/m2 per day. Average abundance of common loach in stream habitats was higher than in beaver ponds (5.5 and 1.3 ind./m2, respectively). The same was true for its biomass – 6.1 and 1.5 g/m2, respectively. The loach production was 0.05 g/m2 per day. The average biomass of spadefoot tadpoles in the studied water bodies was 25 g/m2. The total mass of all tadpoles in floodplain water bodies was 35051 g. Tadpole production reached 1.7 g/m2 per day. Using previous estimates of the number of metamorphose emerging from the water after metamorphosis, the flux of matter transferred by the spadefoots was calculated. In 2022, this flux was 1331 g per year (wet weight) or 257 g per year (dry weight). During their metamorphosis, the spadefoots transferred a total of 0.65 g per year of eicosapentaenoic and docosahexaenoic acids, which are especially important to terrestrial vertebrates. The number and biomass of grass snakes Natrix natrix inhabiting floodplain water bodies of the Khoper River were estimated. In total, the relative abundance of snakes was at least 8 individuals/ha in the 6,000 m2 territory. The average weight of young-of-year individuals had no differences between sexes and ranged from 10 to 11.1 g. The weight of adult females ranged from 55.1 to 89.4 g, males – from 32.5 to 84.1 g. Based on the data obtained earlier and the material collected in 2022, the biomass of zoobenthos of the model beaver pond was calculated and the intensity of fluxes of amphibiotic insects from this water body was estimated. The total intensity of insect flows from the pond ecosystem was 12.10±1.11 ind./m2 per day, the intensity of biomass flux was 49.23±6.17 mg/m2 per day. The role of Diptera and Ephemeroptera (70.3%) in biomass fluxes from pond ecosystem is the most significant and equipollent. Secondary production losses of zoobenthos in wet weight were 32%. To investigate the nutritional spectrum of amphibian tadpoles, the composition of fatty acids in biomass of marsh frog tadpoles from two habitat types, beaver ponds and floodplain water bodies, was analyzed. Preliminary statistical analysis showed the presence of differences in PUFA composition in biomass of tadpoles from different habitats. This proves the biotopic variability of tadpole food preferences and indicates the differences of water bodies themselves. Total fatty acid concentrations were higher in beaver ponds than in floodplain ponds (4.64±1.34 and 3.83±1.16 mg/g wet weight, respectively). Significant differences between the two habitats were found for most PUFAs. In particular, tadpoles from floodplain habitats had significantly higher concentrations of bacterial marker acids (15-17BFA, 17:0, 18:1n-7) in their biomass. Higher concentrations of acid markers of cyanobacteria, higher plants (18:2n-6, 18:3n-3), and diatom algae (20:5n-3) were found in tadpoles from beaver ponds, but these differences were not reliable.

Publications