Article

Marina B. Fardeeva, Dr. Sc., Professor of General Ecology Department of the Kazan Federal University (420008, Russia, Kazan, Kremlevskaya Street, 18); iD ORCID: http://orcid.org/0000-0002-9912-5326; e-mail: orchis@inbox.ru
Nelli A. Chizhikova, PhD, Associate Professor of Ecosystem Modelling Department of the Kazan Federal University (420008, Russia, Kazan, Kremlevskaya Street, 18); iD ORCID: http://orcid.org/0000-0002-9969-9207; e-mail: nelly.chizhikova@kpfu.ru

Fardeeva M.B., Chizhikova N.A. 2023. Dynamics of spatial and ontogenetic structure of Cephalanthera rubra (Orchidaceae) populations in the east of European Russia (Middle Volga Region). Nature Conservation Research 8(2): 52–71. https://dx.doi.org/10.24189/ncr.2023.015

The assessment of the spatial and functional features of rare species populations without considering the ontogenetic groups, which are being rarely distinguished at international literature, does not give a complete understanding of the current status of populations and prospects of their development under various management conditions. This paper is aimed to determine the status of a threatened orchid species, Cephalanthera rubra, at the eastern border of its range (Republic of Tatarstan, European Russia). For this purpose, a complex of various population parameters was used. Ontogenetic groups of C. rubra individuals have been reliably identified on the basis of morphometric traits of reproductive and vegetative organs. The obtained results showed that the fruit set is low, ranging at average from 24% for young reproductive individuals (g1) to 39% for mid-mature reproductive individuals (g2); it reflects prospects for seed reproduction of this species at the eastern edge of its range. The abundance dynamics of populations has a fluctuation type; it is related to climatic factors of the growing season. So, we found its significant positive correlations with air humidity (from r = 0.6 to r = 0.7) and precipitation (from r = 0.5 to r = 0.6), and a negative correlation with temperature (from r = -0.5 to r = -0.6). In the Republic of Tatarstan, the base spectrum of C. rubra populations is of the centred type, 1:10:51:38 (j:im:v:g); it corresponds to the general ontogenetic spectrum of rhizomatous orchids. The spatial-ontogenetic structure of populations, and especially its dynamics, reflects the intraspecific relationships of various ontogenetic groups involved in maintaining the stability of C. rubra population in space and time. Under optimal conditions, the spatial structure of all individuals and reproductive groups is characterised by a spatial randomness, which probably reduces intraspecific competition. In contrary, pre-reproductive groups form aggregations with 0.5–0.9-m radius in microloci, favourable for seed germination. A characteristic feature of the spatial structure is the formation of aggregations of reproductive and pre-reproductive individuals with a 0.7–1.0-m radius with a 0.2–0.4-m zone of the random spatial positioning of individuals, which aims to reduce intraspecific competition between them. The probability of meeting an individual of another ontogenetic group increases towards the periphery of the formed aggregation. In C. rubra populations, the abundance and density of individuals, and the fruit set decrease in pessimal conditions of landslides, soil erosion, and habitat shading. Under these conditions, pre-reproductive individuals do not form aggregations, nor aggregations with reproductive individuals. In general, the spatial structure of a population depends on the life-form type of the species, the mechanism of spatial growth of underground organs; it is considered a diagnostic sign of the population status.

morphometry, ontogenetic groups, ontogenetic structure, orchids, population dynamics, Republic of Tatarstan, spatial structure

Received: 24.08.2022. Revised: 23.01.2023. Accepted: 15.02.2023.

Baddeley A., Turner R. 2005. spatstat: An R Package for Analyzing Spatial Point Patterns. Journal of Statistical Software 12(6): 1–42. DOI: 10.18637/jss.v012.i06
Baddeley A., Rubak E., Turner R. 2015. Spatial Point Patterns: Methodology and Applications with R. London: Chapman and Hall/CRC Press. 828 p.
Bakin O.V., Rogova T.V., Sitnikova A.P. 2000. Vascular plants of the Republic of Tatarstan. Kazan: Kazan Federal University. 496 p. [In Russian]
Barlybaeva M.Sh., Ishmuratova M.M. 2017. Cephalanthera rubra (L.) Rich. in the South-Ural State Nature Reserve. In: Biological systems: stability, principles and mechanisms of functioning. Nizhny Tagil: Russian State Vocational Pedagogical University. P. 61–67. [In Russian]
Barlybayeva M.Sh., Kildiyarova G.N., Suyundukov I.V., Ishmuratova M.M. 2021. Assessment of coenopopulations Epipactis atrorubens in nature reserves of Republic of Bashkortostan. IOP Conference Series: Earth and Environmental Science 817: 012013. DOI: 10.1088/1755-1315/817/1/012013
Barman D., Devadas R. 2013. Climate change on orchid population and conservation strategies: A review. Journal of Crop and Weed 9(2): 1–12.
Bilz M., Kell S.P., Maxted N., Lansdown R.V. 2011. European Red List of Vascular Plants. Luxembourg: Publications Office of the European Union. 130 p. DOI: 10.2779/8515
Blinova I.V. 2009. Biology of orchids in the northeast of Fennoscandia and strategies for their survival on the northern border of distribution. Dr. Sc. Thesis Abstract. Moscow. 44 p. [In Russian]
Blinova I.V. 2014. On CSR- and R–K-strategies of rare vascular plant species in Murmansk Region (Russia). Proceedings of the Karelian Research Centre of the Russian Academy of Sciences 4(19): 83–95. [In Russian]
Brzosko E., Wróblewska A. 2003. Genetic variation and clonal diversity in island Cephalanthera rubra populations from the Biebrza National Park, Poland. Botanical Journal of the Linnean Society 143(1): 99–108. DOI: 10.1046/j.1095-8339.2003.00201.x
Brzosko E., Wróblewska A. 2013. Genetic diversity of nectar-rewarding Platanthera chlorantha and nectarless Cephalanthera rubra. Botanical Journal of the Linnean Society 171(4): 751–763. DOI: 10.1111/boj.12025
Chen I.C., Hill J.K., Ohlemüller R., Roy D.B., Thomas C.D. 2011. Rapid Range Shifts of Species Associated with High Levels of Climate Warming. Science 333(6045): 1024–1026. DOI: 10.1126/science.1206432
Chung M.Y., Nasson J.D. 2007. Spatial demographic and genetic consequences of harvesting within populations of the terrestrial orchid Cymbidium goeringii. Biological Conservation 137(1): 125–137. DOI: 10.1016/j.biocon.2007.01.021
Chung M.Y., Nasson J.D., Chung M.G. 2005. Spatial genetic structure in populations of the terrestrial orchid Orchis cyclochila (Orchidaceae). Plant Systematics and Evolution 254(3): 209–219. DOI: 10.1007/s00606-005-0341-5
Czarnecka B. 2008. Spatiotemporal Patterns of Genets and Ramets in a Population of Clonal Perennial Senecio rivularis: Plant Features and Habitat Effects. Annales Botanici Fennici 45(1): 19–32. DOI: 10.5735/085.045.0103
Dinerstein E., Olson D., Joshi A., Vynne C., Burgess N.D., Wikramanayake E., Hahn N., Palminteri S., Hedao P., Noss R., Hansen M., Locke H., Ellis E.C., Jones B., Barber C.V., Hayes R., Kormos C., Martin V., Crist E., Sechrest W., Price L., Baillie J.E.M., Weeden D., Suckling K., Davis C., Sizer N., Moore R., Thau D., Birch T., Potapov P., Turubanova S., Tyukavina A., de Souza N., Pintea L., Brito J.C., Llewellyn O.A., Miller A.G., Patzelt A., Ghazanfar S.A., Timberlake J., Klöser H., Shennan-Farpón Y., Kindt R., Lillesø J.B., van Breugel P., Graudal L., Voge M., Al-Shammari K.F., Saleem M. 2017. An Ecoregion-Based Approach to Protecting Half the Terrestrial Realm. Bioscience 67(6): 534–545. DOI: 10.1093/biosci/bix014
Dodd M. 2011. Anacamptis morio population variability in time and space. In: Protection and cultivation of orchids. Moscow: KMK Scientific Press Ltd. P. 148–153.
Egorova N.Yu., Egoshina T.L. 2018. New locations of rare vascular plant species on cut-over peat lands (on the example of Kirov Region). Samara Journal of Science 7(3): 35–41. [In Russian]
Fardeeva M.B. 2022. The impact of various factors on the population dynamics of Epipactis atrorubens (Hoffm. ex Bernh.) Bess. in the Middle Volga region. IOP Conference Series: Earth and Environmental Science 1045: 012117. DOI: 10.1088/1755-1315/1045/1/012117
Fardeeva M.B. 2016. Cephalanthera rubra (L.) Rich. In: Red Data Book of the Republic of Tatarstan. Kazan: Idel-Press. P. 434–435. [In Russian]
Fardeeva M.B., Chizhikova N.A., Krasilnikova O.V. 2010a. Features of the space-age structure of rhizomatous orchids under anthropogenic impact. In: Theoretical problems of ecology and evolution. Theory of areas: species, communities, ecosystems. Togliatti: Institute of Ecology of the Volga Basin. P. 195–201. [In Russian]
Fardeeva M.B., Chizhikova N.A., Krasilnikova O.V. 2010b. Long-term dynamics of ontogenetic and spatial structure in Cypripedium calceolus L. populations. Uchenye Zapiski Kazanskogo Universiteta. Seriya Estestvennye Nauki 152(3): 159–173. [In Russian]
Fardeeva M.B., Chizhikova N.A. 2019. Features of Spatial and Temporal Dynamics of Tuberous Orchid Populations. Contemporary Problems of Ecology 12(1): 71–82. DOI: 10.1134/S1995425519010062
Fardeeva M.B., Chizhikova N.A., Biryuchevskaya N.V., Rogova T.V., Savel'ev A.A. 2009. Mathematical approaches to the analysis of the spatial-age structures of tussock herb species. Russian Journal of Ecology 40(4): 233–240. DOI: 10.1134/S106741360904002X
Fardeeva M.B., Rogova T.V. 2012. Methods of investigation in spatial and age structure of plant population. Rastitelnye Resursy 48(4): 597–613. [In Russian]
Foremnik K., Krawczyk W., Surmacz B., Malicki M., Suchan T., Gazda A., Pielech R. 2021. Effects of Forest Stand Structure on Population of Endangered Orchid Species Cypripedium calceolus L. Journal for Nature Conservation 64: 126089. DOI: 10.1016/j.jnc.2021.126089
Galiano E.F. 1982. Pattern detection in plant populations through the analysis of plant-to-all-plants distances. Vegetatio 49: 39–43. DOI: 10.1007/BF00051564
Gilian L.D., Endredi A., Zsinka B., Nemenyi A., Nagy J.G.Y. 2019. Morphological and reproductive trait-variability of a food deceptive orchid, Cephalanthera rubra along different altitudes. Applied Ecology and Environmental Research 17(3): 5619–5639. DOI: 10.15666/aeer/1703_56195639
Greig-Smith P. 1961. The use of pattern analysis in ecological investigations. Recent Advances in Botany 2: 1354–1358.
Grigoryeva N.M., Zaugolnova L.B., Smirnova O.V. 1977. Features of the spatial structure of cenopopulations of some plant species. In: Cenopopulations of plants: development and relationships. Moscow: Nauka. P. 20–36. [In Russian]
Harper J.L. 1977. Population biology of plants. London: Academic Press. 892 p.
Ilyina V.N. 2018. Ontogenetic structure of coenotic populations of some rare representatives of the Orchidaceae under anthropogenic pressure (Samara Region). Samarskaya Luka: problems of regional and global ecology 27(4): 34–39. [In Russian]
Ishbirdina A.R., Ishmuratova M.M., Zhirnova T.V. 2005. Life strategies of Cephalanthera rubra (L.) Rich. on the territory of the Bashkir State Nature Reserve. Vestnik of Lobachevsky University of Nizhni Novgorod 1(9): 85–98. [In Russian]
Ishmuratova M.M., Suyundukov I.V., Ishbirdina A.R., Barlybaeva M.Sh., Nabiullin M.I., Krivosheeva M.M. 2019. Orchids (Orchidaceae Juss.) in the Southern Urals: ecological-phytocoenotic and population characteristics, anthropotolerance, antecology. Bulletin of Perm University. Biology 3: 240–257. DOI: 10.17072/1994-9952-2019-3-240-257 [In Russian]
Istomina E.Yu. 2020. Orchid (Orchidaceae Juss.) on Inza pool territory (central part of Volga hill) // International Research Journal 2(92): 124–129. DOI: 10.23670/IRJ.2020.92.2.024 [In Russian]
IUCN. 2022. The IUCN Red List of Threatened Species. Version 2022-2. Available from https://www.iucnredlist.org
Jacquemyn H., Brys R., Vandepitte K., Honnay O., Roldán-Ruiz I., Wiegand T. 2007. A spatially explicit analysis of seedling recruitment in the terrestrial orchid Orchis purpurea. New Phytologist 176(2): 448–459. DOI: 10.1111/j.1469-8137.2007.02179.x
Jacquemyn H., Wiegand T., Vandepitte K., Brys R., Roldán-Ruiz I., Honnay O. 2009. Multigenerational analysis of spatial structure in the terrestrial, food-deceptive orchid Orchis mascula. Journal of Ecology 97(2): 206–216. DOI: 10.1111/j.1365-2745.2008.01464.x
Jakubska-Busse A., Pielech R., Szczęśniak E. 2014. The Extinction of Terrestrial Orchids in Europe: Does Disappearance of Cephalanthera Rich., 1817 (Orchidaceae, Neottieae) Species Show Pattern Consistent with the Elevation Gradient?. Life Science Journal 11(4): 140–144.
Kazazaeva M.T. 2009. Ecological and biological features and diversity of orchids in Western Transbaikalia: analysis of the structure and state of the gene pool. PhD Thesis Abstract. Ulan-Ude. 18 p. [In Russian]
Kolomyts E.G., Rozenberg G.S., Kolkutin V.I., Yunina V.P., Sidorenko M.V., Orlova M.V., Surova N.A. 1995. Landscape ecology of the Volga River basin in the system of global climatic changes (Prognostic atlas-monograph). Nizhnii Novgorod: Inter-Volga. 163 p. [In Russian]
Lang D. 1980. Orchids of Britain. A field guide. Oxford: Oxford University Press. 213 p.
Lenoir J., Gégout J.C., Marquet P.A., de Ruffray P., Brisse H.A. 2008. Significant Upward Shift in Plant Species Optimum Elevation During the 20^th Century. Science 320(5884): 1768–1771. DOI: 10.1126/science.1156831
Markov M.V. 2012. Population biology of plants. Moscow: KMK Scientific Press Ltd. 388 p. [In Russian]
Martynova A.L. 2021. Features of the spatial-ontogenetic structure of the populations of Zygophyllum pinnatum (Zygophyllaceae). In: Ecology: facts, hypotheses, models. Ekaterinburg: Alfa Print. P. 107–111. [In Russian]
Nazarov V.V. 2016. Seed productivity of European orchids. II. Seed productivity of flower and the inflorescence at Cephalanthera species in the Crimea. Ekosistemy 8(38): 49–58. [In Russian]
Nilsson L.A. 1983. Mimesis of bellflower (Campanula) by the red helleborine orchid Cephalanthera rubra. Nature 305(5937): 799–800. DOI: 10.1038/305799a0
Order. 2016. Order of the Ministry of Natural Resources of the Russian Federation of 23.05.2016 №306 on approval of the Procedure for Maintaining the Red Data Book of the Russian Federation. Legislative acts of the Russian Federation, №2, article 325, №25, Article 3811. [In Russian]
Osmanova G.O. 2021. Ontogenetic structure of coenopopulations of Cephalanthera rubra. In: Biological diversity of natural and anthropogenic landscapes: study and protection. Astrakhan: Astrakhan State University. P. 64–68. [In Russian]
Parzych A., Sobisz Z. 2013. Preliminary ecology research on Epipactis atrorubens (Hoffm.) Besser on the Słowińskie Coast (Northern Poland). Ecological Questions 18: 21–32. DOI: 10.2478/ecoq-2013-0002
Prokhorov V., Rogova T., Kozhevnikova M. 2017. Vegetation Database of Tatarstan. Phytocoenologia 47(3): 309–313. DOI: 10.1127/phyto/2017/0172
R Core Team. 2022. R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. Available from http://www.R-project.org
Raventós J., Mujica E., Wiegand T., Bonet A. 2011. Analyzing the spatial structure of Broughtonia cubensis (Orchidaceae) populations in the dry forests of Guanahacabibes, Cuba. Biotropica 43(2): 173–182. DOI: 10.1111/j.1744-7429.2010.00684.x
Red Data Book of the Republic of Tatarstan. Kazan: Idel-Press, 2016. 760 p. [In Russian]
Ripley B.D. 1977. Modelling spatial patterns. Journal of the Royal Statistical Society: Series B (Methodological) 39(2): 172–212. DOI: 10.1111/J.2517-6161.1977.TB01615.X
Sanaeva L.V. 2020. Study of the dynamics of the plant communities and groupings including rare and endangered species of vascular plants in the Mordovia state nature reserve in 1986–1990. Proceedings of the Mordovia State Nature Reserve 25: 3–49. [In Russian]
Senchugova M.A., Chugunov G.G., Khapugin A.A. 2017. Population-based studies of Iris aphylla (Iridaceae), Cephalanthera rubra (Orchidaceae) and Lilium martagon (Liliaceae) on the east of the Republic of Mordovia in 2016. Proceedings of the Mordovia State Nature Reserve 18: 206–214. [In Russian]
Smirnova O.V. 2010. Basic concepts of ecosystem ecology from the point of view of the population paradigm. In: Principles and methods of biodiversity conservation. Yoshkar-Ola: Mari State University. P. 46–48. [In Russian]
Soule M.E. (Ed.). 1986. Conservation Biology: The Science of Scarcity and Diversity. Oxford: Oxford University Press. 584 p.
Summerhayes V. 1951. Wild Orchids of Britain. London: Collins. 366 p.
Tatarenko I.V. 1996. Orchids of Russia: life forms, biology, conservation issues. Moscow: Argus. 207 p. [In Russian]
Urbanavichute S.P. 2016. New location of Cephalanthera rubra (L.) Rich. in the Kerzhensky State Nature Reserve. Proceedings of the State Nature Biosphere Reserve «Kerzhensky» 8: 174–180. [In Russian]
Vakhrameeva M.G., Varlygina T.I., Kulikov P.V. 1996. Cephalanthera longifolia. In: Biological flora of the Moscow Region. Vol. 12. Moscow: Argus. P. 48–59. [In Russian]
Vakhrameeva M.G., Tatarenko I.V., Varlygina T.I., Torosyan G.K., Zagulskii M.N. 2008. Orchids of Russia and Adjacent Countries (within the borders of the former USSR). Liechtenstein: A.R.G. Gantner Verlag Ruggell. 690 p.
Varlygina T.I. 2011. Protection of orchids of Russia at the state and regional levels. In: Protection and cultivation of orchids. Moscow: KMK Scientific Press Ltd. P. 76–80. [In Russian]
Vasilevich V.I. 1969. Statistical methods in geobotany. Leningrad: Nauka. 232 p. [In Russian]
Wang C.Y., Zhao L.J., Meng S.Y. 2022. Spatial distribution pattern and protection strategy for orchids in landslide mass of the Wanglang National Nature Reserve. Biodiversity Science 30(2): 21313. DOI: 10.17520/biods.2021313
Wiegand T., Gunatilleke S., Gunatilleke N., Okuda T. 2007. Analyzing the spatial structure of a Sri Lankan tree species with multiple scales of clustering. Ecology 88(12): 3088–3102. DOI: 10.1890/06-1350.1
Zaugolnova L.B. 1994. Structure of seed plant populations and problems of their monitoring. Dr. Sc. Thesis Abstract. St. Petersburg. 72 p. [In Russian]
Zenkina T.E. 2016. Study of cenopopulations of dominant species of halophytic communities in the Kuma-Manych depression (Republic of Kalmykia). PhD Thesis Abstract. Togliatti. 20 p. [In Russian]
Zenkina T.E., Ilina V.N. 2017. Structure features of Artemisia salsoloides Willd. (Asteraceae) coenotic populations in the Samara Region. Samara Journal of Science 6(4): 41–47. DOI: 10.17816/snv201764108 [In Russian]
Zenkina T.E., Ilina V.N. 2021a. The assessment of the spatial ontogenetic structure of the coenopopulation Oxytropis floribunda (Pall.) DC. in undisturbed coenoses (on the territory of the Samara Region) // Samara Journal of Science 10(1): 74–79. DOI: 10.17816/snv2021101110 [In Russian]
Zenkina T.E., Ilina V.N. 2021b. State of cenopopulations of some rare species of plants of Samara region in the territory of nature monument of regional importance «Sernovodny Shikhan». Bulletin of Udmurt University. Series Biology. Earth Sciences 31(1): 5–15. DOI: 10.35634/2412-9518-2021-31-1-5-15 [In Russian]
Zenkina T.E., Ilyina V.N. 2019. Characteristics of the structure of coenopopulation Hedysarum grandiflorum Pall. (Fabaceae) using spatial statistics methods. Samarskaya Luka: problems of regional and global ecology 28(1): 55–62. DOI: 10.24411/2073-1035-2019-10181 [In Russian]
Zhirnova T.V., Vakhrameeva M.G. 2008. Cephalanthera rubra (L.) Rich. In: Red Data Book of the Russian Federation (plants and fungi). Moscow: KMK Scientific Press Ltd. P. 360–361. [In Russian]