A comparative study of Epipactis atrorubens in two different forest communities of the Middle Urals, Russia

Abstract

The objective of this study was to compare eco-physiological and morphological parameters of a regionally endangered orchid species, Epipactis atrorubens (Hoffm. ex Bernh.) Bess., growing in two forest communities (on serpentine and granite outcrops) of the Middle Urals, Russia. Biodiversity, dominance, and phytocoenosis studies showed the colonization of a wide range of plant species on both sites. The physicochemical properties of the soil, chemical composition and morphological features of E. atrorubens, growing under technogenic conditions (asbestos deposits), on serpentine outcrops and in the natural environment of the granite massif were studied for the first time. The serpentine substrate differed from the granite one by its greater stoniness, circumneutral pH and lower contents of available nitrogen and phosphorus. Extremely high concentrations of magnesium were found in the serpentine soil, some 79 times higher than in the granite substrate. High concentrations of nickel (94 times), chromium (59 times), cobalt (17 times), and iron (4 times) were found in the serpentine substrate, higher than in the granite substrate. The differences between the sites for available metal contents and for root and shoot metal contents were significantly less. Concentrations of most of the metals in the roots were higher than in the shoots. Despite higher metal concentrations and lower nitrogen and phosphorus levels in serpentine soils, E. atrorubens had a larger population and greater viability compared to those growing on granite. Plants on serpentine outcrops were characterized by the formation of a larger number of fruits, greater root lengths and thicker leaf blades, compared to plants on granites. The well-developed orchid mycorrhizae contributed to the survival of this species under unfavorable serpentine conditions. Hence, serpentine outcrops formed due to the mining of asbestos could be a suitable substrate for the light-demanding E. atrorubens due to its capacity to adapt to dry, rocky, nutrient-depleted soils and limited competition from other plants.

Keywords

Orchids / Forest phytocoenosis / Serpentine / Granite / Metal accumulation

References

[1] Adamowski W. Expansion of native orchids in anthropogenous habitats. Pol Bot Stud, 2006, 22: 35-44.

[2] Bekuzarova SA, Bome NA, Opalko AI, Weisfeld LI. Temperate crop science and breeding ecological and genetic studies, 2016, New York: Apple Academic Press

[3] Bilz M, Kell SP, Maxted N, Lansdown RV. European red list of vascular plants, 2011, Luxembourg: Publications Office of the European Union.

[4] Borisova G, Chukina N, Maleva M, Prasad MNV. Ceratophyllum demersum L. and Potamogeton alpinus Balb. from Iset’ river, Ural region, Russia differ in adaptive strategies to heavy metals exposure—a comparative study. Int J Phytoremediat, 2014, 16: 621-633.

[5] Brady KU, Kruckeberg AR, Bradshaw HD. Evolutionary ecology of plant adaptation to soils. Annu Rev Ecol Evol Syst, 2005, 36: 243-266.

[6] Buttler PK. Field guide to orchids of Britain and Europe, 1991, Swindon: The Crowood Press.

[7] Delforge P. Orchids of Europe, North Africa and the Middle East, 2006, London: A & C Black.

[8] Djordjević V, Tsiftsis S, LakuŠić D, Stevanović V. Niche analysis of orchids of serpentine and non-serpentine areas: implications for conservation. Plant Biosyst, 2016, 150(4): 710-719.

[9] Ellenberg H, Weber HE, Dull R, Wirth V, Werner W, Paulissen D. Ecological indicator values of Central European plant species. Scr Geobot, 1991, 18: 1-248.

[10] Filimonova EI, Lukina NV, Glazyrina MA, Borisova GG, Maleva MG, Chukina NV. Endangered orchid plant Epipactis atrorubens on serpentine and granite outcrops of Middle Urals, Russia: a comparative morphophysiological study. AIP Conf Proc, 2019, 2063: 040016.

[11] Hens H, Jäkäläniemi A, Tali K, Efimov P, Kravchenko AV, Kvist L. Genetic structure of a regionally endangered orchid, the dark red helleborine (Epipactis atrorubens) at the edge of its distribution. Genetica, 2017, 145(2): 209-221.

[12] Jurkiewicz A, Turnau K, Mesjasz-Przybylowicz J, Przybylowicz W, Godzik B. Heavy metal localisation in mycorrhizas of Epipactis atrorubens (Hoffm.) Besser (Orchidaceae) from zink mine tailings. Protoplasma, 2001, 218: 117-124.

[13] Kazakou E, Dimitrakopoulos PG, Baker AJM, Reeves RD, Troumbis AY. Hypotheses, mechanisms and trade-offs of tolerance and adaptation to soils: from species to ecosystem level. Biol Rev, 2008, 83: 495-508.

[14] Kazakou E, Adamidis GC, Baker AJM, Reeves RD, Godino M, Dimitrakopoulos PG. Species adaptation in soils in Lesbos Island (Greece): metal hyperaccumulation and tolerance. Plant Soil, 2010, 332: 369-385.

[15] Red Book of Sverdlovsk region: animals, plants, fungi (2008) Korytin NS (ed) Basko, Ekaterinburg (in Russian)

[16] Kristy U, Kruckeberg A, Bradshaw H Jr. Evolutionary ecology of plant adaptation to serpentine soils. Annu Rev Ecol Evol Syst, 2005, 36: 243-266.

[17] Kumar A, Maiti SK, Tripti Prasad MNV, Singh RS. Grasses and legumes facilitate phytoremediation of metalliferous soils in the vicinity of an abandoned chromite-asbestos mine. J Soils Sed, 2017, 17(5): 1358-1368.

[18] Landolt E (1977) Okologische zeigerwerte zur schweizer flora. Veroff. Geobot. Inst. Rubel. H.64. Stiftung Riibel, Zurich

[19] Magurran AE. Ecological diversity and its measurement, 1988, London: Croom Helm

[20] Maiti SK. Ecorestoration of the coalmine degraded lands, 2013, New York: Springer

[21] Mamaev SA, Knyazev MS, Kulikov PV, Filippov EG (2004) Orkhidnye Urala (Orchids of Ural), Ural. Otd. Ross. Akad. Nauk, Ekaterinburg (in Russian)

[22] Marschner H. Mineral nutrition of higher plants, 1995 2 London: Academic Press.

[23] M-MVI-80 (2008) Methods for performing measurements of the mass fraction of elements in soil, ground and bottom sediment samples using atomic emission and atomic adsorption spectrometry. St. Petersburg (in Russian)

[24] Mukhopadhyay S, Rana V, Kumar A, Maiti SK. Biodiversity variability and metal accumulation strategies in plants spontaneously inhibiting fly ash lagoon. India. Environ Sci Pollut Res, 2017, 24(29): 22990-23005.

[25] Prasad R. Determination of potentially available nitrogen in soils—a rapid procedure. Plant Soil, 1965, 23(2): 261-264.

[26] Rajakaruna N, Boyd RS. Gibson D. Serpentine soils. Oxford bibliographies in ecology, 2014, New York: Oxford University Press

[27] Rewicz A, Bomanowska A, Shevera M, Kurowski J, Krason K, Zielinska K. Cities and disturbed areas as man-made shelters for orchid communities. Not Bot Horti Agrobot Cluj Napoca, 2017, 45(1): 126-139.

[28] Shefferson R, Kull T, Tali K. Mycorrhizal interactions of orchids colonizing Estonian mine tailings hills. Am J Bot, 2008, 95(2): 156-164.

[29] Smith SE, Read DJ. Mycorrhizal symbiosis, 2008 3 New York: Academic Press.

[30] Smith TM, Smith RL. Elements of ecology, 2012 9d Harlow: Pearson.

[31] Swarts DN, Dixon WD. Terrestrial orchid conservation in the age of extinction. Ann Bot, 2009, 104: 543-556.

[32] Tešitelová T, Tešitel J, Jersáková J, Říhová G, Selosse MS. Simbiotic germination capability of four Epipactis species (Orchidaceae) is broader than expected from adult ecology. Am J Bot, 2012, 99(6): 1020-1032.

[33] Tsiftsis S, Tsiripidis I, Karagiannakidou V, Alifragis D. Niche analysis and conservation of the orchids of east Macedonia (NE Greece). Acta Oecol, 2008, 33: 27-35.

[34] Vakhrameeva MG, Tatarenko IV, Varlygina TI, Torosyan GK, Zagulskii MN. Orchids of Russia and adjacent countries (within the borders of the former USSR), 2008, Ruggell: A.R.G. Gantner.

[35] Van der Ent A, Rajakaruna R, Boyd RS, Echevarria G, Repin R, Williams D. Global research on ultramafic (serpentine) ecosystems (8th international conference on serpentine ecology in Sabah, Malaysia): a summary and synthesis. Aust J Bot, 2015, 63: 1-16.