Ecological and physiological peculiarities of bryophytes on a post-technogenic salinized territory

  • O. V. Lobachevska Institute of Ecology of the Carpathians of the National Academy of Sciences of Ukraine
  • N. Y. Kyyak Institute of Ecology of the Carpathians of the National Academy of Sciences of Ukraine
  • I. V. Rabyk Institute of Ecology of the Carpathians of the National Academy of Sciences of Ukraine
Keywords: salt stress; tailings storage; moss reproduction; carbohydrates; cation exchange capacity; plant ecomorphogenesis.

Abstract

Taxonomic, biomorphological and ecological structures of bryophytes, their reproductive strategy and the main mechanisms of tolerance in the conditions of salinization were investigated. Bryophytes are the pioneers that have colonized the territory of a tailing storage that holds liquid waste from potassium-magnesium concentrate production of the Mining and Chemical Enterprise "Polymineral". Due to excess salts, the soil solution in the shore area of the tailing pond acquires high osmotic pressure. Three experimental plots which differed significantly in the level of the substrate salinity were laid at the distance of 3, 6 and 9 m from the reservoir for experimental studies. Water extracts of the substrates from the test sites showed the highest concentrations for sulfates – 10.4–64.6 mg Eq/100 g of soil and chlorides – 7.6–43.3 mg Eq/100 g of soil. It was established that the investigated areas of the tailing storage territory differed in the biochemical activity of the substrate, which was evaluated by its redox potential. On the areas of the uncovered substrate it was the lowest – 230 mV, which indicates anaerobiosis in conditions of very high salinization and moisture. Higher ROP values were determined at the sites of bryophyte cover distribution – 295–330 mV. The aim of the study was to determine the features of taxonomic, biomorphological and ecological structures of bryophytes, their reproductive strategy and to establish the main mechanisms of adaptation to the conditions of salinization on the tailing storage territory. 24 species and 3 varieties of bryophytes, belonging to 12 families and 16 genera were found on the shore of the tailing storage pond. The results of biomorphological and ecological analysis of bryophytes indicate the uneven conditions of the habitats and their considerable ecological plasticity. Among the bryophytes, mesophytes, xeromesophytes and meso-eutrophs, eutrophs with a life-form of low dense and loose turf dominated. In salinization conditions, dioicous acrocarpous mosses prevailed, the fertile turf of which, depending on the influence of abiotic factors, differed significantly in the number of sexual shoots, their ratio and productivity. Bulbils were found only on the tips of Bryum argenteum shoots. Along with Salicornia europaea L., a euhalophyte, the leading role in the initial stage of overgrowth of the tailing storage area most often belonged to Didymodon rigidulus, Bryum argenteum, Funaria hygrometrica and Barbula unguiculata. The process of formation of bryophyte cover occurred along a gradient of decrease in salt concentration at the experimental sites. Adaptation of bryophytes to substrate salinity is due to a change in metabolic processes, which is manifested in an increase of the total content of carbohydrates and an increase of the cation exchange capacity of moss cell walls, which is the primary barrier that reduces the toxic effect of ions under salt stress.

References

Aronson, J., & Alexander, S. (2013). Ecosystem restoration is now a global priority: Time to roll up our sleeves. Restoration Ecology, 21, 293–296.


Ball, B. A., & Guevara, J. N. (2014). The nutrient plasticity of moss-dominated crust in the urbanized Sonoran Desert. Plant and Soil, 389, 225–235.


Bates, J. W., Wibbelmann, M. H., & Proctor, M. C. F. (2009). Salinity responses of halophytic bryophytes determined by chlorophyll fluorometry. Journal of Bryology, 31, 11–19.


Batista, W. V. S. M., Pôrto, K. C., & Santos, N. D. (2018). Distribution, ecology, and reproduction of bryophytes in a humid enclave in the semiarid region of Northeastern Brazil. Acta Botanica Brasilica, 32(2), 303–313.


Baughman, J. T., Payton, A. C., Paasch, A. E., Fisher, K. M., & McDaniel, S. F. (2017). Multiple factors influence population sex ratios in the Mojave Desert moss Syntrichia caninervis. American Journal of Botany, 104(5), 733–742.


Bazylevych, N. Y., & Pankova, E. Y. (1970). Uchet zasolennyih pochv. Metodicheskie rekomendatsii po melioratsii solontsov i uchetu zasolennyih pochv [Accounting for saline soils. Methodical recommendations for melioration and accounting for saline soils]. Kolos, Moscow (in Russian).


Blamey, F. P. С. (1990). Role of root cation-exchange capacity in differential aluminium tolerance of litus species. Journal of Plant Nutrition, 13(6), 729–745.


Boiko, M. F. (2014). The second checklist of Bryobionta of Ukraine. Chornomorski Botanical Journal, 10(4), 426–487.


Bueno de Mesquita, C. P., Knelman, J. E., King, A. J., Farrer, E. C., Porazinska, D. L., Schmidt, S. K., & Suding, K. N. (2017). Plant colonization of moss-dominated soils in the alpine: Microbial and biogeochemical implications. Soil Biology and Biochemistry, 111, 135–142.


Carter, D. W., & Arocena, J. M. (2000). Soil formation under two moss species in sandy materials of Central British Columbia (Canada). Geoderma, 98(3–4), 157–176.


Cortina-Segarra, J., Decleer, K., & Kollmann, J. (2016). Speed restoration of EU ecosystems. Nature, 535, 231.


Ćosić, M., Vujičić, M., Sabovljević, M., & Sabovljević, A. (2018). What do we know about salt stress in bryophytes? Plant Biosystems, 9(4), 51–60.


Delgado-Baquerizo, M., Fernando, M. D.-B., Maestre, T., Eldridge, D. J., Bowker, M. A., Jeffries, T. C., & Singh, B. K. (2018). Biocrust-forming mosses mitigate the impact of aridity on soil microbial communities in drylands: Observational evidence from three continents. New Phytologist, 22(3), 824–835.


Douma, J. C., Van Wijk, M. T., Lang, S. I., & Shaver, G. R. (2007). The contribution of mosses to the carbon and water exchange of arctic ecosystems: Quantification and relationships with system properties. Plant, Cell and Environment, 30(10), 1205–1345.


Flowers, T. J., Munns, R., & Colmer, T. D. (2014). Sodium chloride toxicity and the cellular basis of salt tolerance in halophytes. Annals of Botany, 115, 419–431.


Garbary, D. J., Miller, A. G., Scrosati, R., Kim, K., & Schofield, W. B. (2008). Distribution and salinity tolerance of intertidal mosses from Nova Scotia. The Bryologist, 111, 282–291.


García, E. L., Rosenstiel, T. N., Graves, C., Shortlidge, E. E., & Eppley, S. M. (2016). Distribution drivers and physiological responses in geothermal bryophyte communities. American Journal of Botany, 103(4), 625–634.


Gao, B., Li, X., Zhang, D., Liang, Y., Yang, H., Chen, M., Zhang, Y., Zhang, J., & Wood, A. J. (2017). Desiccation tolerance in bryophytes: The dehydration and rehydration transcriptomes in the desiccation-tolerant bryophyte Bryum argenteum. Scientific Reports, 7, 75–87.


Glime, G. M. (2006). Bryophyte ecology. Biological Sciences, Michigan Technological University.


Goffinet, B., Buck, W. R., & Shaw, A. J. (2009). Morphology, anatomy and classification of the Bryophyta. In: Bryophyte Biology. Cambridge University Press. Pp. 55–138.


Greenwood, J. L., & Stark, L. R. (2014). The rate of drying determines the extent of desiccation tolerance in Physcomitrella patens. Functional Plant Biology, 41(5), 460–467.


Haig, D. (2016). Living together and living apart: The sexual lives of bryophytes. Philosophical Transactions of the Royal Society: Biological Sciences, 19(371), 1706–1715.


Ignatov, M. S., & Ignatova, E. A. (2003). Flora mkhov srednej chasti evropejskoj Rossii [Moss flora of Middle European Russia]. 1: Sphagnaceae – Hedwigiaceae. KMK, Arctoa, Moscow. Vol. 11(1), 1–608 (in Russian).


Ignatov, M. S., & Ignatova, E. A. (2004). Flora mkhov srednej chasti evropejskoj Rossii [Moss flora of Middle European Russia]. 2: Fontinalaceae – Amblistegiaceae. KMK, Arctoa, Moscow. Vol. 11(1), 609–944 (in Russian).


Jackson, T. A. (2015). Weathering, secondary mineral genesis, and soil formation caused by lichens and mosses growing on granitic gneiss in a boreal forest environment. Geoderma, 12, 78–91.


Janicka-Russak, M., & Kabała, K. (2015). The role of plasma membrane H+-ATPase in salinity stress of plants. In: Lёuttge, U., & Beyschlag, W. (Eds.). Progress in Botany. International Publishing Switzerland, Springer. Pp. 76–92.


Karpinets, L., Lobachevska, O., & Baranov, V. (2016). Vplyv mokhiv na mikroklimatychni umovy edafotopiv porodnyh vidvaliv i i’hni adaptacijni reakcii [Influence of mosses on microclimatic conditions of edaphotopes of rock dumps and their adaptive responses]. Studia Biologica, 10(3–4), 119–128 (in Ukrainian).


Karpinets, L. I., Lobachevska, O. V., & Sokhanchak, R. R. (2017). Ekolohichna struktura epiheinykh synuzii mokhopodibnykh na porodnykh vidvalakh Chervonohradskoho hirnychopromyslovoho raionu [Ecological structure of epigeic synusiae of mosses on rock dumps of Chervonograd industrial mining region]. Ukrainian Botanical Journal, 74(2), 154–162 (in Ukrainian).


Kul’bachko, Y. L., Didur, O. O., Loza, I. M., Pakhomov, O. E., & Bezrodnova, O. V. (2015). Environmental aspects of the effect of earthworm (Lumbricidae, Oligochaeta) tropho-metabolic activity on the pH buffering capacity of remediated soil (steppe zone, Ukraine). Biology Bulletin, 42, 899–904.


Kyyak, N. Y., & Khorkavtsiv, Y. D. (2015). Adaptatsiya bryophitiv do vodnoho deficytu na terytoriji vidvalu vydobutku sirky [Adaptation of the bryophytes to water deficit in the dump area at sulphur deposit sites]. Ukrainian Botanical Journal, 72(6), 566–573 (in Ukrainian).


Kyyak, N. Y., & Baik, O. L. (2016). Role of the bryophyte cover in accumulation of organic carbon and biogenic elements in technogenic substrate on the territory of sulfur deposit. Studia Biologica, 10(3–4), 71–82.


Kyyak, N. Y., & Khorkavtsiv, Y. D. (2016). Otsinka okysniuvalnoho stresu mokhu Pohlia nutans (Hedw.) Lindb. zalezhno vid vplyvu hravitatsii [Estimation of the oxidative stress in moss Pohlia nutans (Hedw.) Lindb. depending on the influence of gravity]. Space Science and Technology, 22(4), 58–66 (in Ukrainian).


Kyyak, N. Y., Baik, O. L., & Kit, N. A. (2017). Morfo-fiziolohichna adaptatsija bryofitiv do ekolohichnych factoriv na devastovbanych terytoriajach vydobutku sirky [Morpho-physiological adaptation of bryophytes to environmental factors on the devastated territories of sulphur extraction]. ScienceRise: Biological Science, 5(8), 33–38 (in Ukrainian).


Lobachevska, O., Kyjak, N., Khorkavtsiv, O., Dovgalyuk, A., Kit, N., Klyuchivska, O., Stoika, R., Ripetsky, R., & Cove, D. (2005). Influence of metabolic stress on the inheritance of cell determination in the moss, Pottia intermedia. Cell Biology International, 29(3), 181–186.


Lobachevska, O. V. (2014). Mokhopodibni yak model doslidzhennia ekofiziolohichnoi adaptatsii do umov pryrodnoho seredovyshcha [Bryophytes as a model for the study of ecophysiological adaptation to environmental conditions]. Chornomorski Botanical Journal, 10(1), 48–60 (in Ukrainian).


Lobachevska, O. V., & Sokhanchak, R. R. (2017). Reproduktyvna stratehiia adventyvnoho mokhu Campylopus introflexus (Leucobryaceae, Bryophyta) na terytoriiakh hirnychodobuvnykh pidpryiemstv Lvivshchyny [Reproductive strategy of the alien moss Campylopus introflexus (Leucobryaceae, Bryophyta) in areas of mining enterprises in Lviv Region]. Ukrainian Botanical Journal, 74(1), 46–55 (in Ukrainian).


Lobachevska, O. V., Kyyak, N. Y., & Khorkavtsiv, Y. D. (2019). Morfofunktsionalni osoblyvosti klityn protonemy Weissia tortilis Spreng. z riznoiu chutlyvistiu do hravitatsii [Morpho-functional peculiarities of the moss Weissia tortilis Spreng. protonemata cells with different gravisensitivity]. Space Science and Technology, 25(2), 60–70 (in Ukrainian).


Maestre, F. T., Escolar, C., Bardgett, R. D., Dungait, J. A., Gozalo, B., & Ochoa, V. (2015). Warming reduces the cover and diversity of biocrust-forming mosses and lichens, and increases the physiological stress of soil microbial communities in a semi-arid Pinus halepensis plantation. Frontiers in Microbiology, 25(6), 858–865.


Nikolaichuk, V. I., Belchhazi, V. I., & Bilyk, P. P. (2000). Spetspraktykum z fiziolohii i biokhimii roslyn [Special practice on plants physiology and biochemistry]. Patent, Uzhhorod (in Ukrainian).


Pakhomov, O., Kulbachko, Y., Didur, O., & Loza, I. (2008). Mining dump rehabilitation: The potential role of bigeminate-legged millipeds (Diplopoda) and artificial mixed-soil habitats. In: Apostol, I., Barry, D. L., Coldewey, W. G., & Reimer, D. W. G. (Eds.). Optimisation of disaster forecasting and prevention measures in the context of human and social dynamics. NATO science for peace and security series E-human and societal dynamics. Chisinau, Moldova, 52, 163–171.


Rabyk, І. V., Lobachevska, O. V., Shcherbachenko, O. I., & Danilkіv, І. S. (2017). Mohopodibni jak indykatory vidnovlennja posttehnogennyh landshaftiv vydobutku sirky [Bryophytes as indicators of recovery posttechnogenic landscapes of sulfur extraction]. Chornomorski Botanical Journal, 13(4), 468–480 (in Ukrainian).


Reed, S. C., Coe, K. K., Sparks, J. P., Housman, D. C., Zelikova, T. J., & Belnap, J. (2012). Changes to dryland rainfall result in rapid moss mortality and altered soil fertility. Nature Climate Change, 2, 752–755.


Rykovsky, G. F., & Maslovsky, O. M. (2004). Flora of Belarus. Bryophyta. Technalohija, Minsk.


Sadasivam, S., & Manickam, A. (2007). Biochemical methods. New Age International, New Delhi.


Seitz, S., Nebel, M., Goebes, P., Käppeler, K., Schmidt, K., Shi, X., Song, Z., Webber, C. L., Weber, B., & Scholten, T. (2017). Bryophyte-dominated biological soil crusts mitigate soil erosion in an early successional Chinese subtropical forest. Biogeosciences, 14, 5775–5788.


Shcherbachenko, O. I., Rabyk, I. V., & Lobachevska, О. V. (2015). Uchast mokhopodibnykh u renaturalizatsii devastovanykh terytorii Nemyrivskoho rodovyshcha sirky (Lvivska obl.) [Role of bryophytes in renaturalization of the devastated areas of Nemyriv sulfur deposit (Lviv Region)]. Ukrainian Botanical Journal, 72(6), 596–602 (in Ukrainian).


Stark, L. R. (2017). Ecology of desiccation tolerance in bryophytes: A conceptual framework and methodology. The Bryologist, 120(2), 129–164.


Stassart, J. M., Neirinckx, L., & Dejaegere, R. (1981). The interactions between monovalent cations during their adsorption on isolated cell walls and adsorption by intact barley roots. Annals of Botany, 47(9), 647–652.


Trites, M., & Bayley, S. E. (2009). Vegetation communities in continental boreal wetlands along a salinity gradient. Implications for oil sands mining reclamation. Aquatic Botany, 91, 27–39.


Vilmundardóttir, O. K., Sigurmundsson, F. S., Møller Pedersen, G. B., Belart, J. M. C., Kizel, F., Falco, N., Benediktsson, J. A., & Gísladóttir, G. (2018). Of mosses and men: Plant succession, soil development and soil carbon accretion in the sub-arctic volcanic landscape of Hekla, Iceland. Progress in Physical Geography: Earth and Environment, 42(6), 765–791.


Wang, X., Liu, Z., & He, Y. (2008). Responses and tolerance to salt stress in bryophytes. Plant Signaling and Behavior, 3(8), 516–518.


Whitehead, J., Wittemann, M., & Gronberg, N. (2018). Allelopathy in bryophytes – a review. Lindbergia, 41, 1–7.


Zechmeister, H. G. (2005). Bryophytes of continental salt meadows in Austria. Journal of Bryology, 27(4), 297–302.


Zhao, Y., Qin, N., Weber, B., & Xu, M. (2014). Response of biological soil crusts to raindrop erosivity and underlying influences in the hilly Loess Plateau region, China. Biodiversity and Conservation, 23, 1669–1686.

Published
2019-10-24
Section
Articles

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