Long-term dynamics of flora of karst lakes: Changes and current state

E. A. Belyakov; E. V. Garin

doi:10.15421/011825

E. A. Belyakov Papanin Institute for Biology of Inland Waters of the Russian Academy of Sciences http://orcid.org/0000-0001-8465-9037
E. V. Garin Cherepovets State University http://orcid.org/0000-0002-0199-9405

Keywords: eutrophication; vascular plants; adventive species; rare plants; structure of flora; floristic richness

Abstract

Long-term observations of the rates and pattern of changes in flora and vegetation contribute to understanding of one of the most important contemporary global problems, the eutrophication of water bodies. In this study, using classical floristic methods, we attempt to determine (for a period of almost 80 years) the nature and possible causes of changes in the floristic composition of the lakes of karst origin, Velikoe and Parovoe (Pustinskaya lake-river system, the right bank of Nizhny Novgorod oblast). The paper shows that over a long period of observations a significant transformation of the vegetation cover has occurred in the lakes. The process was accompanied by the disappearance of a number of native species and appearance of others, including adventitious ones (for example, Elodea canadensis Michx., Zizania latifolia (Griseb.) Stapf, Bidens frondosa L. and Epilobium adenocaulon Hausskn.). The weak saturation of the flora with adventive species indicates that the reservoirs are subject to moderate anthropogenic transformation. This is also indicated by the presence of characteristic indicator species, for example, Najas minor All., Glyceria fluitans (L.) R. Br., Hydrocharis morsus-ranae L. and Stratiotes aloides L. in the plant communities. In addition, the studied water bodies are subject to a further increase in the degree of eutrophication. This can be judged by scattered records of Potamogeton trichoides Cham. et Schlecht., the disappearance of a number of species (such as Elatine alsinastrum L. and Callitriche hermaphroditica L.), as well as the presence of a significant number of macrophyte indicators of the eutrophic state of water bodies. We suggest that a gradual increase in the trophicity of the studied water bodies is due to a combination of anthropogenic impact (water withdrawal for economic needs, recreational load), natural and climatic features of the region (alternation of high and low water periods) and the natural succession processes associated with the current fundamental changes in the conditions of the runoff formation in the Volga River basin. As a result of studies conducted by authors in 2014–2015, it has been shown that in general the taxonomic and ecological structures of the flora of both lakes are quite diverse and traditional for the territory and the European part of Russia. Meanwhile, the flora of these two reservoirs insignificantly differs in taxonomic composition, which is due to their individual morphometric characteristics, the physical and chemical properties of the aquatic environment, and the nature of the anthropogenic load. At the same time, the equilibrium balance of coastal and aquatic plants in the flora of Lake Parovoe (in contrast to Lake Velikoe) indicates a degree of successional stability of its floristic complex.

References

Astashin, A. E., Badin, M. M., Kartashov, A. Y., Goryachev, A. S., Voznesenskaya, M. V., Karabanov, A. D., & Pashkin, M. N. (2016). Morfometricheskie harakteristiki ozyor Parovoe, Kruglen'koe, Glubokoe gosudarstvennogo prirodnogo biologicheskogo zakaznica Pustynskiy (Nizhegorodskaya oblast') [Morphometric characteristics of the lakes Parovoe, Kruglen’koe, Glubokoe of the state natural biological wildlife area “Pustynsky” (Nizhny Novgorod region)]. Meždunarodnyj Naučno-Issledovatel'skij Žurnal, 50, 49–54 (in Russian).

Averkiev, D. S. (1954). Istoriya razvitiya rastitelnogo pokrova Gorkovskoy oblasti i eyo botaniko-geograficheskoe delenie [The history of the development of plant cover in the Gorkiy oblast and its phytogeographical division]. Uchyonye Zapiski Gorkovskogo Gosudarstvennogo Universiteta. Seriya Biologicheskaya, 25, 119–136 (in Russian).

Bakka, S. V., & Kiselyeva, N. Y. (2008). Osobo ohranyaemye prirodnye territorii Nizhegorodskoy oblasti: Annotirovannyy perechen [Protected areas in Nizhny Novgorod oblast: Annotated list]. Minprirody Nizhegorodskoi oblasti, Nizhnii Novgorod (in Russian).

Bazarova, B. B., & Pronin, N. M. (2010). Elodea canadensis Michxaux na granice mirovogo vodorazgela Ledivitogo i Tihogo okeanov [Elodea canadensis Michxaux oh the border of world watershed of Arctic and Pacific oceans]. Russian Journal of Biological Invasions, 3, 2–12 (in Russian).

Beklioglu, M., Romo, S., Kagalou, I., Quintana, X., & Becares, E. (2007). State of the art in the functioning of shallow Mediterranean lakes: Workshop conclusions. Hydrobiologia, 584(1), 317–326.

Belavskaya, A. P. (1994). Vodnye rasteniya Rossii i sopredel'nykh gosudarstv [Aquatic plants of Russia and neighboring countries]. Russian Academy of Sciences, Saint Petersburg (in Russian).

Belote, R. T., Jones, R. H., & Wieboldt, T. F. (2012). Compositional stability and diversity of vascular plant communities following logging disturbance in Appalachian forests. Ecological Applications, 22(2), 502–516.

Belyakov, E. A., Garin, E. V., & Okhapkin, A. G. (2015). Flora ozyorno-rechnogo kompleksa reki Seryozha Pustynskogo zakaznika (Nizhegorodskaya obl., Arzamasskiy rayon) [Flora of lake-river complex Seryozha in the Pustyn preserve (Nizhny Novgorod region, Arzamas oblast)]. In: Proceedings of VII All-Russian conference with international participation on aquatic macrophytes “Hydrobotany 2015”. Filigran, Yaroslavl, 72–75 (in Russian).

Belyakov, E. A., Garin, E. V., & Okhapkin, A. G. (2017). Flora of karst lakes in the Pustynsky State Nature Reserve (Nizhny Novgorod oblast). Biosystems Diversity, 25(3), 174–180.

Birykova, O. V., Schestakova, A. A., Belyakov, E. A., & Garin, E. V. (2017). O rasprostranenii Caulinia minor (All.) Coss. et Germ. (Hydrocharitaceae, Liliopsida) na territorii Nizhegorodskoy oblasti [On the distribution of Caulinia minor (All.) Coss. et Germ. (Hydrocharitaceae, Liliopsida) on the territory of the Nizhny Novgorod region]. Povolzhskiy Journal of Ecology, 3, 251–259 (in Russian).

Bornette, G., Henry, C., Barrat, M. H., & Amoros, C. (1994). Theoretical habitat templets species traits, and species richness: Aquatic macrophytes in the Upper Rhône River and its floodplain. Freshwater Biology, 31(3), 485–505.

Byng, J. W., Chase, M. W., Christenhusz, M. J. M., Fay, M. F., Judd, W. S., Mabberley, D. J., Sennikov, A. N., Soltis, D. E., Soltis, P. S., & Stevens, P. F. (2016). An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV. Botanical Journal of the Linnean Society, 181(1), 1–20.

Cao, J. J., Wang, Y., & Zhu, Z. L. (2012). Growth response of the submerged macrophyte Myriophyllum spicatum to sediment nutrient levels and water-level fluctuations. Aquatic Biology, 17(3), 295–303.

Carpenter, S. R., & Lodge, D. M. (1986). Effects of submersed macrophytes on ecosystem processes. Aquatic Botany, 26, 341–370.

Chambers, P. A., Lacoul, P., Murphy, K. J., & Thomaz, S. M. (2008). Global diversity of aquatic macrophytes in freshwater. Hydrobiologia, 595(1), 9–26.

Cherepanov, S. K. (1995). Sosudistye rasteniya Rossii i sopredelnyh gosudarstv (v predelah byvshego SSSR) [Vascular plants of Russia and the adjacent states (within the former USSR)]. Mir i Semya – 95, St. Petersburg (in Russian).

Christenhusz, M. J. M., & Chase, M. W. (2014). Trends and concepts in fern classification. Annals of Botany, 113(4), 571–594.

Christenhusz, M. J. M., Reveal, J. L., Farjon, A., Gardner, M. F., Mill, R. R., & Chase, M. W. (2011). A new classification and linear sequence of extant gymnosperms. Phytotaxa, 19, 55–70.

Clayton, J., & Edwards, T. (2006). Aquatic plants as environmental indicators of ecological condition in New Zealand lakes. Hydrobiologia, 570, 147–151.

Coops, H., Beklioglu, M., & Crisman, T. L. (2003). The role of water-level fluctuations in shallow lake ecosystems – workshop conclusions. Hydrobiologia, 506(1–3), 23–27.

Deegan, B. M., White, S. D., & Ganf, G. G. (2007). The influence of water level fluctuations on the growth of four emergent macrophyte species. Aquatic Botany, 86(4), 309–315.

Dhanam, S., & Elayaraj, B. (2015). Distribution and composition of aquatic macrophytes in Santhapettai Lake of Villupuram District in Tamil Nadu. International Letters of Natural Sciences, 47, 74–81.

Dubyna, D. V., Stoyko, S. М., Sytnik, S. М., Tasenkevich, L. А., Shelyag-Sosonko, Y. V., Geyny, S., Groudova, Z., Gusak, S., Otygelova, G., & Erzhabkova, О. (1993). Makrofity – indikatory izmeneniy prirodnoy sredy [Macrophytes indicators of changes of natural environment]. Naukova Dumka, Kiev (in Russian).

Dzhus, M. A. (2011). Ryaska turionoobrazuyushchaya (Lemna turionifera Landolt, Lemnaceae) – novyy vid dlya flory Belarusi i Nacional'nogo parka «Narochanskiy» [Lemna turionifera Landolt (Lemnaceae) – a new species for the flora of Belarus and the National Park "Narochansky"]. In: Osobo ohranyaemye prirodnye territorii Belarusi. Belorusskiy Dom pechati, Minsk. Vypusk 6, 68–80 (in Russian).

Egertson, C. J., Kopaska, J. A., & Downing, J. A. (2004). A century of change in macrophyte abundance and composition in response to agricultural eutrophication. Hydrobiologia, 524, 145–156.

Evangelista, H. B. A., Thomaz, S. M., & Umetsu, C. A. (2014). An analysis of publications on invasive macrophytes in aquatic ecosystems. Aquatic Invasions, 9(4), 521–528.

Franklin, J., Serra-Diaz, J. M., Syphard, A. D., & Regan, H. M. (2016). Global change and terrestrial plant community dynamics. Proceedings of the National Academy of Sciences of the United States of America, 113(14), 3725–3734.

Gubanov, I. A., Kiseleva, K. V., Novikov, V. S., & Tihomirov, V. N. (2002). Illyustrirovannyy opredelitel' rasteniy Sredney Rossii [Illustrated manual on Central Russia plants]. Vol. 1. KMK Press, Moscow (in Russian).

Gubanov, I. A., Kiseleva, K. V., Novikov, V. S., & Tihomirov, V. N. (2013). Illyustrirovannyy opredelitel' rasteniy Sredney Rossii [Illustrated manual on Central Russia plants]. Vol. 2. KMK Press, Moscow (in Russian).

Higgins, S. I., & Cain, M. L. (2002). Spatially realistic plant metapopulation models and the colonization-competition trade-off. Journal of Ecology, 90(4), 616–626.

Kapitonova, O. A., & Dyukina, G. R. (2008). Novyy vid Typha (Typhaceae) iz Udmurtii [A new species of the genus Typha (Typhaceae) from Udmurtia]. Botanical Journal, 93(7), 1132–1134 (in Russian).

Katanskaya, V. M. (1981). Vysshaya vodnaya rastitelnost kontinentalnyh vodoemov SSSR: Metody izucheniya [Higher aquatic vegetation of continental water bodies of the USSR: Study methods]. Nauka, Leningrad (in Russian).

Krasnaya kniga Nizhegorodskoy oblasti (2005). Tom 2. Sosudistye rasteniya, vodorosli, lishayniki, griby [The Red Book of Nizhny Novgorod oblast. Vol. 2. Vascular plants, algae, lichens, fungi]. Komitet Okhrany Prirody i Upravlenie Prirodopol'zovaniya Nizhegorodskoy Oblasti, Nizhny Novgorod (in Russian).

Kravchenko, A. V., Timofeeva, V. V., Chkalov, A. V., Byalt, V. V., Molodkina, K. D., & Fadeeva, M. A. (2016). Novye dlya Karelii vidy sosudistyh rasteniy [New vascular plant species in the republic of Karelia]. Transactions of Karelian Research Centre of the Russian Academy of Sciences, 3, 76–83.

Lacoul, P., Freedman, B., & Clair, T. (2011). Effects of acidification on aquatic biota in Atlantic Canada. Environmental Reviews, 19, 429–460.

Landolt, E. (1975). Morphological differentiation and geographical distribution of the Lemna gibba – Lemna minor group. Aquatic Botany, 1, 345–363.

Lehmann, A., & Lachavanne, J. B. (1999). Changes in the water quality of Lake Geneva indicated by submerged macrophytes. Freshwater Biology, 42(3), 457–466.

Lenssen, J., & de Kroon, H. (2005). Abiotic constraints at the upper boundaries of two Rumex species on a freshwater flooding gradient. Journal of Ecology, 93, 138–147.

Lisitsyna, L. I., & Artyemenko, V. I. (1990). Bidens frondosa L. – novyy vid flory Nizhnego Povolzh'ya [Bidens frondosa L. – a new species for the flora of Lower Volga]. Bulletin of Moscow Society of Naturalists. Biological Series, 95(4), 110–111 (in Russian).

Lisitsyna, L. I., Papchenkov, V. G., & Artyemenko, V. I. (2009). Flora vodoyomov Volzhskogo basseina: Opredelitel sosudistyh rasteniy [Flora of water bodies of the Volga river basin: Identification guide of vascular plants]. KMK Press, Moscow (in Russian).

Lukina, E. V. (1982). O dinamike flory i rastitelnosti ozera Velikogo Pustynskogo Gorkovskoy oblasti [On the dynamics of flora and vegetation in the lakes Velikoe of Pustynskiy of Gorky oblast]. In: Biologicheskie osnovy povysheniya produktivnosti i ohrana rastitelnyh soobshchestv Povolzhya. Izdatelstvo Gorkovskogo gosudarstvennogo Universiteta, Gorkiy. Pp. 71–77 (in Russian).

Luo, F. L., Jiang, X. X., Li, H. L., & Yu, F. H. (2016). Does hydrological fluctuation alter impacts of species richness on biomass in wetland plant com-munities? Journal of Plant Ecology, 9(4), 434–441.

Mäemets, H., Palmik, K., Haldna, M., Sudnitsyna, D., & Melnik, M. (2010). Eutrophication and macrophyte species richness in the large shallow North-European Lake Peipsi. Aquatic Botany, 92(4), 273–280.

Maevskiy, P. F. (2014). Flora sredney polosy evropeyskoy chasti Rossii [Flora of the temperate zone of the european part of the Russia]. KMK Press, Moscow (in Russian).

Maltseva, S. Y., & Bobrov, А. А. (2017). Chuzherodnye vidy sosudistyh rasteniy Rybinskogo vodohranilishcha (verhnyaya Volga, Rossiya) [Alien species of vascular plants of the Rybinsk reservoir (upper Volga, Russia)]. Russian Journal of Biological Invasions, 3, 30–37 (in Russian).

Mavrodiev, E. V., & Kapitonova, O. A. (2015). Taksonomicheskiy sostav rogozovykh (Typhaceae) flory evropeiskoy chasti Rossii [Taxonomic composition of Typhaceae of the flora of European Russia]. Novitates Systematicae Plantarum Vascularium, 46, 5–24 (in Russian).

Mavrodiev, E. V., & Sukhorukov, A. P. (2006). Nekotorye novye i kriticheskie taksony flory ktaynego yugo-vostoka Evropy [Some new and critical taxa of the flora of outermost European South-East]. Bulletin of Moscow Society of Naturalists. Biological Series, 111(1), 77–83 (in Russian).

Melnikova, A. P. (2014). Ob osobennostyah obrazovaniya samyh krupnyh karstovyh ozyor Nizhegorodskoy oblasti [On the peculiarities of formation of the largest karst lakes in the Nizhny Novgorod oblast]. In: Fundamental'nye i prikladnye issledovaniya: Problemy i rezul'taty [Fundamental and applied research: Problems and results]. CRNS, Novosibirsk. Pp. 8–12 (in Russian).

Nikitina, I. G. (1982). Rasprostranenie kubyshki zhyoltoy Nuphar lutea (L.) Smith na Pustynskih ozyorah Gor'kovskoy oblasti v svyazi s ohranoy ehtogo vida [The distribution of Nuphar lutea (L.) Smith on the Pustyn lakes of the Gorky Region in connection with the protection of this species]. In: Biologicheskie osnovy povysheniya produktivnosti i ohrana rastitelnyh soobshchestv Povolzhya. Izdatelstvo Gorkovskogo Gosudarstvennogo Universiteta, Gorkiy. Pp. 67–70 (in Russian).

Papchenkov, V. G. (2001). Rastitelnyy pokrov vodoyomov Srednego Povolzhya [Vegetation cover of water bodies and water courses of the Middle Volga region]. CMP MUBiNT, Yaroslavl (in Russian).

Peintinger, M., Prati, D., & Winkler, E. (2007). Water level fluctuations and dynamics of amphibious plants at Lake Constance: Long-term study and simulation. Perspectives in Plant Ecology, Evolution and Systematics, 8(4), 179–196.

Pereira, S. A., Trindade, C. R., Albertoni, E. F., & Palma-Silva, C. (2012). Aquatic macrophytes as indicators of water quality in subtropical shallow lakes, Southern Brazil. Acta Limnologica Brasiliensia, 24(1), 52–63.

Pirini, C. B., Karagiannakidou, V., & Charitoni, S. (2011). Abundance, diversity and distribution of macrophyte communities in neighboring lakes of different trophic states and morphology in North-Central Greece. Archives of Biological Sciences, 63(3), 763–774.

Raunkiaer, C. (1937). Plant life forms. Clarendon Press, Oxford.

Riis, T., & Hawes, I. (2002). Relationships between water level fluctuations and vegetation diversity in shallow water of New Zealand lakes. Aquatic Botany, 74(2), 133–148.

Santamaria, L. (2002). Why are most aquatic plants widely distributed? Dispersal, clonal growth and small-scale heterogeneity in a stressful environment. Acta Oecologica, 23, 137–154.

Sender, J. (2012). The dynamics of macrophytes in a lake in an agricultural landscape. Limnological Review, 12(2), 93–100.

Seo, A., Lee, K., Kim, B., & Choung, Y. (2014). Classifying plant species indicators of eutrophication in Korean lakes. Paddy and Water Environment, 12(1), 29–40.

Sharma, R. C., & Singh, S. (2017). Macrophytes of Sacred Himalayan Lake Dodi Tal, India: Quantitative and diversity analysis. Biodiversity International Journal, 1(4), 1–11.

Shchennikov, A. P. (1964). Vvedenie v geobotaniku [Introduction to geobotanica]. Izdatelstvo Leningradskogo Universiteta, Leningrad (in Russian).

Smirnova, A. D., & Nikitina, I. G. (1972). Novoe vo flore i rasprostranenii vodnykh rasteniy v Gor'kovskoy oblasti [New in flora and spreading of aquatic plants of Gorki district]. Botanicheskii Zhurnal, 57(3), 354–356 (in Russian).

Smirnova, A. D., Lukina, E. V., & Nikitina, I. G. (1975). Materialy po dinamike flory i rastitelnosti ozera Parovogo iz sistemy Pustynskih ozyor Gorkovskoy oblasti [The materials on the dynamics of flora and vegetation of the lake Parovoe from the system Pustynsky lakes of Gorky oblast]. In: Biologicheskie osnovy povysheniya produktivnosti i ohrany lesnyh, lugovyh i vodnyh fitocenozov. Vol. 4. Gorkovskii Gosudarstvennyi Universitet imeni N. I. Lobachevskogo, Gorkiy. Pp. 42–52 (in Russian).

Teneva, I., Gecheva, G., Cheshmedjiev, S., Stoyanov, P., Mladenov, R. & Belkinova, D. (2014). Ecological status assessment of Skalenski Lakes (Bulgaria). Biotechnology and Biotechnological Equipment, 28(1), 82–95.

Terentev, A. A., & Kolkutin, V. I. (2004). Klimat kontsa XX veka v sredney polose Nizhegorodskoy oblasti [The climate of the late twentieth century in Central Nizhny Novgorod region]. Vektor-TiS, Nizhny Novgorod (in Russian).

Teteryuk, B. Y. (2012). Flora i rastitelnoct' drevnikh ozyor evropeiskogo Severo-Vostoka Rossii [Flora and vegetation of ancient lakes of the European northeast of Russia]. Nauka, Saint Petersburg (in Russian).

Vargot, E. V., Khapugin, A. A., Chugunov, G. G., Ivashina, A. A., Silaeva, T. B., & Kiryukhin, I. V. (2012). Dopolneniya k flore Respubliki Mordoviya [Additions to the flora of Mordovia]. Bulletin of Moscow Society of Naturalists. Biological Series, 117(3), 73–74 (in Russian).

Vizer, A. M., & Kipriyanova, L. M. (2010). Nahodka vodyanogo orekha Trapa natans L. s. l. (Trapaceae) v Novosibirskoy oblasti [Finding of Trapa natans L. s. l. (Trapaceae) in Novosibirsk region]. Turczaninowia, 13(3), 67–69 (in Russian).

Vorobyev, P. M. (1943). Vodno-bolotnaya rastitelnost ozera Velikogo bliz sela Pustyn, Chernuhinskogo raiona, Gorkovskoi oblasti [Wetland vegetation the Velikoe lake near the village of Pustyn, Chernuhinsk district, Gorkiy oblast]. Uchyonye Zapiski Gorkovskogo Gosudarstvennogo Universiteta. Seriya Biologicheskaya, 2, 36–43 (in Russian).

Vretare, V., Weisner, S. E., Strand, J. A., & Granéli, W. (2001). Phenotypic plasticity in Phragmites australis as a functional response to water depth. Aquatic Botany, 69(2–4), 127–145.

Wang, P., Zhang, Q., Xu, Y.-S., & Yu, F.-H. (2016). Effects of water level fluctuation on the growth of submerged macrophyte communities. Flora, 223, 83–89.

Wantzen, K. M., Rothhaupt, K. O., Mörtl, M., Cantonati, M., Tóth, L., & Fischer, P. (2008). Ecological effects of water-level fluctuations in lakes: An urgent issue. Hydrobiologia, 613, 1–4.

Xu, N. N., Tong, X., Tsang, P. K. E., Deng, H., & Chen, X. Y. (2011). Effects of water depth on clonal characteristics and biomass allocation of Halophila ovalis (Hydrocharitaceae). Journal of Plant Ecology, 4(4), 283–291.

Yang, X.-E., Wu, X., Hao, H.-L., & He, Z.-L. (2008). Mechanisms and assessment of water eutrophication. Journal of Zhejiang University Science B, 9(3), 197–209.

Yu, L.-F., & Yu, D. (2009). Responses of the threatened aquatic plant Ottelia alismoides to water level fluctuations. Fundamental and Applied Limnology, 174(4), 295–300.

Zarubina, E. Y., & Sokolova, M. I. (2016). Transformatsiya struktury rastitel'nogo pokrova Manzherokskogo ozera (Respublika Altai) za 35-letniy period [Transformation of the plant cover structure of Manzherokskoe Lake (West Altai) over 35 years]. Tomsk State University Journal of Biology, 4(36), 47–61 (in Russian).

Zhang, X. K., Liu, X. Q., & Wang, H. Z. (2015). Effects of water level fluctuations on lakeshore vegetation of three subtropical floodplain lakes, China. Hydrobiologia, 747(1), 43–52.

Zhang, X., Liu, X., & Ding, Q. (2013). Morphological responses to water-level fluctuations of two submerged macrophytes, Myriophyllum spicatum and Hydrilla verticillata. Journal of Plant Ecology, 6(1), 64–70.

Zhmylev, P. Y., Alekseev, Y. E., & Morozova, O. V. (2017). Biologicheskoe raznoobrazie rasteniy Moskovskoy oblasti [Biological diversity of plants in Moscow region]. Gosudarstvennyi universitet "Dubna", Dubna (in Russian).

Zohary, T., & Ostrovsky, I. (2011). Ecological impacts of excessive water level fluctuations in stratified freshwater lakes. Inland Waters, 1, 47–59.