Pollination and floral biology of Adonis vernalis L. (Ranunculaceae) – a case study of threatened species

Bożena Denisow, Małgorzata Wrzesień, Anna Cwener

Abstract


Although the knowledge of pollination systems of rare and threatened species is one of the principles for development of optimal conservation and management strategies, the data about their pollination requirements are scarce or incomplete. Different problems are listed (xerothermic habitat disappearance, overgrowing of patches, plant biology i.e., slow plant growth, problems with seed germination) among the possible causes of Adonis vernalis being threatened, but until now no consideration was given to the flowering biology and pollination.

The observations of flowering biology of A. vernalis (Ranunculaceae), a clonal species, were conducted in an out-of-compact-range population, in the Lublin Upland, Poland (51°18'55" N, 22°38'21" E), in 2011–2013. The reproductive potential of A. vernalis is related to the population age structure, pollination syndrome, and breeding system. The flowers exhibit incomplete protogyny. The dichogamy function is supported by different (biological, morphological) mechanisms. Stigma receptivity occurred about one day before anthers started shedding self-pollen, and pollen viability was increasing gradually during the flower life-span (66.3% in distal anthers vs. 77.3% in proximal). The decrease in pollen production and in pollen viability coincided with the lowest degree of seed set, irrespective of the pollination treatment. Pollen vectors are necessary for efficient pollination, as the proportion of pistils setting fruits after open pollination (41–82.1%) was significantly higher compared to spontaneous self-pollination (only 5.5–12.3%). The pollination requirements together with pollen/ovule ratio (P/O = 501) indicate a facultative xenogamous breeding system in A. vernalis. Therefore, in the conditions of the global lack of pollinators, improper pollination may weaken the population by leading to a decrease in the proportion of recombinants, and in addition to other factors, may accelerate extinction of small A. vernalis populations.


Keywords


Adonis vernalis; self-pollination; open-pollination; pollen; viability; seed set

Full Text:

PDF

References


Bascompte J, Jordano P. Plant-animal mutualistic networks: the architecture of biodiversity. Ann Rev Ecol Syst. 2007;38(1):567–593. http://dx.doi.org/10.1146/annurev.ecolsys.38.091206.095818

Potts SG, Biesmeijer J, Kremen C, Neumann P, Schweiger O, Kunin WE. Global pollinator declines: trends, impacts and drivers. Trends Ecol Evol. 2010;25(6):345–353. http://dx.doi.org/10.1016/j.tree.2010.01.007

Zych M, Jakubiec A. Pollination of Polish red list plants: a preliminary statistical survey. Acta Agrobot. 2008;61(1):85. http://dx.doi.org/10.5586/aa.2008.011

Schemske DW, Husband BC, Ruckelshaus MH, Goodwillie C, Parker IM, Bishop JG. Evaluating approaches to the conservation of rare and endangered plants. Ecology. 1994;75(3):584. http://dx.doi.org/10.2307/1941718

Zych M, Stpiczyńska M. Neither protogynous nor obligatory out-crossed: pollination biology and breeding system of the european red list Fritillaria meleagris L. (Liliaceae). Plant Biol Stuttg. 2012;14(2):285–294. http://dx.doi.org/10.1111/j.1438-8677.2011.00510.x

Zając A, Zając M. Elementy geograficzne rodzimej flory Polski. Cracow: Jagiellonian University; 2009.

Davis SD, Heywood VH, Hamilton AC, editors. Centres of plant diversity. A guide and strategy for their conservation 1. Europe, Africa, Southwest Asia and the Middle East. Cambrige: International Union for Conservation of Nature; 1994.

Schnittler M, Günther KF. Central European vascular plants requiring priority conservation measures – an analysis from national red lists and distribution maps. Biodivers Conserv. 1999;8(7):891–925. http://dx.doi.org/10.1023/A:1008828704456

Denisow B, Wrzesień M, Cwener A. The estimation of Adonis vernalis populations in chosen patches of Lublin Upland. Acta Agrobot. 2008;61(1):3. http://dx.doi.org/10.5586/aa.2008.001

Cwener A. Threatened xerothermic vascular plants in the Działy Grabowieckie mesoregion (Wyżyna Lubelska Upland, SE Poland). In: Mirek Z, Nikel A, editors. Rare, relict and endangered plants and fungi in Poland. Cracow: W. Szafer Institute of Botany, Polish Academy of Sciences; 2009. p. 155–162.

Bilz M, Kell SP, Maxted N, Lansdown RV. European red List of vascular plants. Luxembourg: Publications Office of the European Union; 2011.

Korotchenko I, Peregrym M. Ukrainian steppes in the past, at present and in the future. In: Werger MJ, van Staalduinen MA, editors. Eurasian steppes. Ecological problems and livelihoods in a changing world. Plant and vegetation. Dordrecht: Springer Netherlands; 2012. p. 173–196. (vol 6). http://dx.doi.org/10.1007/978-94-007-3886-7_5

Meusel H, Jäger E, Weinert F. Vergleichende Chorologie der Zentraleropäischen Flora. Jena: Gustav Fischer Verlag; 1965. (vol 3).

Forycka A, Szczyglewska D, Buchwald W. Stock-talking of Adonis vernalis L. in the selected localities in Poland. Bull Bot Gard Mus Collect. 2004;13:55–58.

Sudnik-Wójcikowska B, Moysiyenko II, Slim PA. Dynamics of the flora of windbreaks in the agricultural landscape of steppes in southern Ukraine. Biodiv Res Conserv. 2006;1-2:77–81.

Parnikoza I, Vasiluk A. Ukrainian steppes: current state and perspectives for protection. Ann UMCS Biol. 2011;66(1). http://dx.doi.org/10.2478/v10067-011-0018-0

Świerczyńska S. Problemy zachowania zbiorowisk stepowych na podstawie badań prowadzonych na Lubelszczyźnie. Prądnik: Ojcowski Park Narodowy. Muzeum im. prof. Władysława Szafera; 1990. (vol 2).

Michalik S, Zarzycki K. Management of xerothermic grasslands in Poland: botanical approach. Colloq Phytosociol 1995;24:881–895.

Mihalik E, Gocs K, Kálmán K, Medvegy A. Reproductive success of the individuals with different age in a planted Adonis vernalis L. population. Acta Biol Debr Oecol Hung. 2000;11(1):270–275.

Harper JL. Biologia populacyjna i ekologia organizmów klonalnych. Moduły i rozgałęzienia a pobieranie składników pokarmowych. Wiad Ekol. 1986;32(4):327–359.

Falińska K. Plant population biology and vegetation processes. Cracow: W. Szafer Institute of Botany, Polish Academy of Sciences; 1998.

Czarnecka B. Spatiotemporal patterns of genets and ramets in a population of clonal perennial Senecio rivularis: plant features and habitat effects. Ann Bot Fenn. 2008;45(1):19–32. http://dx.doi.org/10.5735/085.045.0103

Charlesworth D, Charlesworth B. Inbreeding depression and its evolutionary consequences. Ann Rev Ecol Syst. 1987;18(1):237–268. http://dx.doi.org/10.1146/annurev.es.18.110187.001321

Lloyd DG, Webb CJ. The avoidance of interference between the presentation of pollen and stigmas in angiosperms. I. Dichogamy. N Z J Bot. 1986;24(1):135–162. http://dx.doi.org/10.1080/0028825X.1986.10409725

Lloyd DG, Schoen DJ. Self- and cross-fertilization in plants. I. Functional dimensions. Int J Plant Sci. 1992;153(3):358. http://dx.doi.org/10.1086/297040

Sanzol J, Herrero M. The “effective pollination period” in fruit trees. Sci Hortic. 2001;90(1–2):1–17. http://dx.doi.org/10.1016/S0304-4238(00)00252-1

Douglas KL, Cruden RW. The reproductive biology of Anemone canadensis (Ranunculaceae): breeding system and facilitation of sexual selection. Am J Bot. 1994;81(3):314. http://dx.doi.org/10.2307/2445458

Griffin SR, Mavraganis K, Eckert CG. Experimental analysis of protogyny in Aquilegia canadensis (Ranunculaceae). Am J Bot. 2000;87(9):1246. http://dx.doi.org/10.2307/2656717

Dafni A, Firmage D. Pollen viability and longevity: Practical, ecological and evolutionary implications. Plant Syst Evol. 2000;222(1–4):113–132. http://dx.doi.org/10.1007/BF00984098

Larson BMH, Barrett SCH. A comparative analysis of pollen limitation in flowering plants. Biol J Linn Soc. 2000;69(4):503–520. http://dx.doi.org/10.1006/bijl.1999.0372

Aizen MA, Harder LD. Expanding the limits of the pollen limitation concept: effects of pollen quantity and quality. Ecology. 2007;88(2):271–281. http://dx.doi.org/10.1890/06-1017

Denisow B, Wrzesień M. The study of blooming and pollen efficiency of Adonis vernalis L. in xerothermic plant communities. J Apic Sci. 2006;50(1):25–32.

Matuszkiewicz W. Przewodnik do oznaczania zbiorowisk roślinnych Polski. Warsaw: Polish Scientific Publishers PWN; 2001.

Jankowska-Błaszczuk M. Diagnostyczne właściwości struktury przestrzennej populacji Adonis vernalis L. In: Faliński J, editor. Dynamika roślinności i populacji roślinnych. Warsaw: Białowieża Geobotanical Station of Warsaw University; 1991. p. 193–200.

Jankowska-Błaszczuk M. Biologia populacji miłka wiosennego Adonis vernalis L. w rezerwacie “Skowronno”. Ochr Przyr. 1995;52:47–58.

Medvegy A, Szőllősi R, Mihalik E. Temporal floral sex allocation in protogynous Adonis vernalis L. In: Proceedings of the 2nd European Congress of Conservation Biology. Prague: Czech University of Life Sciences, Faculty of Environmental Sciences; 2009. p. 148.

Chmura D, Adamski P, Denisiuk Z. Spatiotemporal aspects of the occurrence of clonal steppe plant Adonis vernalis L. in the southern Poland. Cas Slez Semskeho Muzea A. 2012;61(3):245–250. http://dx.doi.org/http://dx.doi.org/10.2478/v10210-012-0025-z

Dafni A, Maués MM. A rapid and simple procedure to determine stigma receptivity. Sex Plant Reprod. 1998;11(3):177–180. http://dx.doi.org/10.1007/s004970050138

Cruden RW. Pollen-ovule ratios: a conservative indicator of breeding systems in flowering plants. Evolution. 1977;31(1):32. http://dx.doi.org/10.2307/2407542

Gostin IN. Scanning electron microscopy investigations regarding Adonis vernalis L. flower morphology. Analele Univ Din Oradea Fasc Biol. 2009;16(2):80–84.

Stanisz A. Przystępny kurs statystyki z zastosowaniem Statistica na przykładach z medycyny. Cracow: Statsoft Polska; 2007.

Knuth P. Handbuch der Blütenbiologie. Leipzig: Verlag von Wilhelm Engelman; 1898. (vol 2).

Kudo G. Ecological significance of flower heliotropism in the spring ephemeral Adonis ramosa (Ranunculaceae). Oikos. 1995;72(1):14. http://dx.doi.org/10.2307/3546032

Chmura D, Adamski P, Denisiuk Z. How do plant communities and flower visitors relate? A case study of semi-natural xerothermic grasslands. Acta Soc Bot Pol. 2013;82(2):99. http://dx.doi.org/10.5586/asbp.2013.015

Goulson D. Foraging strategies of insects for gathering nectar and pollen, and implications for plant ecology and evolution. Perspect Plant Ecol Evol Syst. 1999;2(2):185–209. http://dx.doi.org/10.1078/1433-8319-00070

Heinrich B, Raven PH. Energetics and pollination ecology. Science. 1972;176(4035):597–602. http://dx.doi.org/10.1126/science.176.4035.597

Chittka L, Thomson JD, Waser NM. Flower constancy, insect psychology, and plant evolution. Naturwissenschaften. 1999;86(8):361–377. http://dx.doi.org/10.1007/s001140050636

Young LW, Wilen RW, Bonham-Smith PC. High temperature stress of Brassica napus during flowering reduces micro- and megagametophyte fertility, induces fruit abortion, and disrupts seed production. J Exp Bot. 2004;55(396):485–495. http://dx.doi.org/10.1093/jxb/erh038

Gusta LV, O’Connor BJ, Bhatty RS. Flax (Linum usitatissimum L.) responses to chilling and heat stress on flowering and seed yield. Can J Plant Sci. 1997;77(1):97–99. http://dx.doi.org/10.4141/P95-205

Rodkiewicz B, Śnieżko R, Fryk B, Niewęgłowska B, Tchórzewska D. Embriologia “Angiospermae” rozwojowa i eksperymentalna. Lublin: Maria Curie-Skłodowska University Press; 1996.

Steffan-Dewenter I, Tscharntke T. Effects of habitat isolation on pollinator communities and seed set. Oecologia. 1999;121(3):432–440. http://dx.doi.org/10.1007/s004420050949

Asikainen E, Mutikainen P. Preferences of pollinators and herbivores in gynodioecious Geranium sylvaticum. Ann Bot. 2005;95(5):879–886. http://dx.doi.org/10.1093/aob/mci094

Klinkhamer PGL, de Jong TJ, Linnebank LA. Small-scale spatial patterns determine ecological relationships: an experimental example using nectar production rates. Ecol Lett. 2001;4(6):559–567. http://dx.doi.org/10.1046/j.1461-0248.2001.00267.x