Floral biology of Senecio macrophyllus M. BIEB. (Asteraceae), a rare Central European steppe plant

Bożenna Czarnecka, Bożena Denisow

Abstract


Knowledge of the flowering phase and plant pollination ecology is very important for understanding the life history of long-lived perennials. In the case of rare species, the information may have implications for conservation practices. Our studies on flower morphology and blooming biology of the vulnerable plant Senecio macrophyllus M. BIEB. were conducted in situ (flowering, activity of insect visitors) in the largest population in SE Poland and in laboratory (light and scanning electron microscopy). The disc florets open diurnally with most intensive anthesis in the early afternoon and attract insect visitors with nectar and pollen. In highly protandrous disc florets, pollen viability decreases in time, whereas stigma receptivity increases. The upper part of the pistil forms a brush-like pollen presenter, covered with unicellular trichomes with chromoplasts. Pollen presentation lasts 4–11 hours per floret, and 8 days in a single head, the main function of which is to extend the availability of male gamets for reproduction. The number of florets per head, the head size, and the number of pollen grains produced per anther, and the pollen grain viability differed significantly between microsites. The finding indicates that, apart from the biotic factors, abiotic conditions may considerably influence generative reproduction of the species. In the study area, the principal visitors of S. macrophyllus flowers were Hymenoptera, with predominance of Apis mellifera (53.4% of visits). The remarkable share of butterflies (13.9%) recognized as the long-distance moving insects may improve the genetic variability of individuals within a fragmented population. A more detailed study is necessary to explain the role of insect visitors in effective pollination and in gene transfer between patches. The assessment of optimal conditions for the generative reproduction is fundamental for the in situ conservation of this rare species.

Keywords


Senecio macrophyllus; flower life-span; insect visitor spectrum; female phase; male phase; pollen production; pollen viability; stigma receptivity

Full Text:

PDF

References


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

Potts SG, Biesmeijer JC, 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

Adams MS, Saravanan JM. Pollination ecology and evolution in Compositae (Asteraceae). Enfield, NH: Science Publishers; 1999.

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

Hiscock S. Self-incompatibility in Senecio squalidus L. (Asteraceae). Ann Bot. 2000;85:181–190. http://dx.doi.org/10.1006/anbo.1999.1058

Comes HP. Selfing ability and male sterility in Senecio vernalis Waldst. et Kit. (Asteraceae) from Israel. Isr J Plant Sci. 1994;42(2):89–103. http://dx.doi.org/10.1080/07929978.1994.10676561

Proctor MCF, Yeo P, Lack A. The natural history of pollination. Portland, OR: Timber Press; 1996.

Zarzycki K, Kaźmierczakowa R, editors. Polish red data book of plants. Pteridophytes and flowering plants. Cracow: W. Szafer Institute of Botany, Polish Academy of Sciences; 2001.

Lowe A, Abbott RJ. A new British species Senecio eboracensis (Asteraceae) another hybrid derivative of S. vulgaris L. and S. squalidus L. Watsonia. 2003;24:375–388.

Grombone-Guaratini MT, Solferini VN, Semir J. Reproductive biology in species of Bidens L. (Asteraceae). Sci Agric. 2004;61(2):185–189. http://dx.doi.org/10.1590/S0103-90162004000200010

Kratochwil A, Beil M, Schwabe A. Complex structure of pollinator-plant interaction-webs: random, nested, with gradients or modules? Apidologie. 2009;40(6):634–650. http://dx.doi.org/10.1051/apido/2009062

Czarnecka B, Kucharczyk M. Senecio macrophyllus M. Bieb. In: Zarzycki K, Kaźmierczakowa R, editors. Polish red data book of plants. Pteridophytes and flowering plants. Cracow: W. Szafer Institute of Botany, Polish Academy of Sciences; 2001. p. 375–377.

Zarzycki K, Szeląg Z. Red list of the vascular plants in Poland. In: Mirek Z, Zarzycki K, Wojewoda W, Szeląg Z, editors. Red list of plants and fungi in Poland. Cracow: W. Szafer Institute of Botany, Polish Academy of Sciences; 2006. p. 9–20.

Czarnecka B. Biology and ecology of the island populations of Senecio rivularis (Waldst. et Kit.) DC. and Senecio umbrosus Waldst. et Kit. Lublin: Maria Curie-Skłodowska University Press; 1995.

Czarnecka B. Large-scale vs. small-scale factors affecting flowering patterns in Senecio macrophyllus M. BIEB., a long-lived perennial. Acta Agrobot. 2006;59(1):233. http://dx.doi.org/10.5586/aa.2006.023

Czarnecka B. The dynamics of the population of a steppe perennial Senecio macrophyllus M. BIEB. during xerothermic grassland overgrowing. Acta Soc Bot Pol. 2009;78(3):247. http://dx.doi.org/10.5586/asbp.2009.032

Czarnecka B. Studies of a steppe perennial Senecio macrophyllus M. Bieb., a “special care” species: from landscape to molecular level. In: Barančoková M, Krajčí J, Kollár J, Belčáková I, editors. Landscape ecology – methods, applications and interdisciplinary approach. Bratislava: Institute of Landscape Ecology, Slovak Academy of Sciences; 2010. p. 559–574.

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

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

Cruden RW. Pollen grains: why so many? Plant Syst Evol. 2000;222(1–4):143–165. http://dx.doi.org/10.1007/BF00984100

Schmitt J. Pollinator foraging behaviour and gene dispersal in Senecio (Compositae). Evolution. 1980;34(5):934. http://dx.doi.org/10.2307/2407999

Herrera CM. Pollinator abundance, morphology, and flower visitation rate: analysis of the “quantity” component in a plant-pollinator system. Oecologia. 1989;80(2):241–248. http://dx.doi.org/10.1007/BF00380158

Pacini E, Franchi GG. Role of the tapetum in pollen and spore dispersal. In: Hesse M, Pacini E, Willemse M, editors. The tapetum. Vienna: Springer Vienna; 1993. p. 1–11. (vol 7). http://dx.doi.org/10.1007/978-3-7091-6661-1_1

Hong L, Shen H, Ye W, Cao H, Wang Z. Secondary pollen presentation and style morphology in the invasive weed Mikania micrantha in South China. Bot Stud. 2008;49:253–260.

Parihar J, Hamal IA, Chibber N, Sharma N. Pollination mechanism and indirect pollen presentation in Artemisia maritima L. Intern J Plant Reprod Biol. 2009;1:191–193.

Haratym W, Weryszko-Chmielewska E. The ecological features of flowers and inflorescences of two species of the genus Petasites Miller (Asteraceae). Acta Agrobot. 2012;65(2):37. http://dx.doi.org/10.5586/aa.2012.056

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

Bożek M. Pollen efficiency and foraging by insect pollinators in three catnip (Nepeta L.) species. J Api Sci. 2003;4:19–25.

Denisow B. Blooming biology and pollen abundance of some Centaurea sp. J Api Sci. 2006;50:13–20.

Denisow B. Pollen production, flowering and insect visits on Euphorbia cyparissias L. and Euphorbia virgultosa Klok. J Api Res. 2009;48(1):50–59. http://dx.doi.org/10.3896/IBRA.1.48.1.11

Howell GJ, Slater AT, Knox RB. Secondary pollen presentation in Angiosperms and its biological significance. Aust J Bot. 1993;41(5):417. http://dx.doi.org/10.1071/BT9930417

Khanduri VP. Variation in anthesis and pollen presentation in plants. Am-Euroasian J Agric Env Sci. 2011;11:843–836.

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

Leins P, Erbar C. On the mechanisms of secondary pollen presentation in the Campanulales-Asterales complex. Bot Acta. 1990;103:87–92.

Ladd PG. Pollen presenters in the flowering plants – form and function. Bot J Linn Soc. 1994;115(3):165–195. http://dx.doi.org/10.1006/bojl.1994.1040

Feldman TS. The plot thickens: does low density affect visitation and reproductive success in a perennial herb, and are these effects altered in the presence of a co-flowering species? Oecologia. 2008;156(4):807–817. http://dx.doi.org/10.1007/s00442-008-1033-y

Ovaskainen O, Smith AD, Osborne JL, Reynolds DR, Carreck NL, Martin AP, et al. Tracking butterfly movements with harmonic radar reveals an effect of population age on movement distance. Proc Natl Acad Sci USA. 2008;105(49):19090–19095. http://dx.doi.org/10.1073/pnas.0802066105

Mitchell RJ, Irwin RE, Flanagan RJ, Karron JD. Ecology and evolution of plant-pollinator interactions. Ann Bot. 2009;103(9):1355–1363. http://dx.doi.org/10.1093/aob/mcp122

Essenberg CJ. Scale-dependent shifts in the species composition of flower visitors with changing floral density. Oecologia. 2012;171(1):187–196. http://dx.doi.org/10.1007/s00442-012-2391-z

Mirek Z, Piękoś-Mirkowa H, Zając A, Zając M, editors. Vascular plants of Poland: a checklist. Cracow: W. Szafer Institute of Botany, Polish Academy of Sciences; 2002.

Bogdanowicz W, Chudzicka E, Pilipiuk I, Skibińska E, editors. Fauna of Poland. Characteristics and checklist of species. Warsaw: Museum of Institute of Zoology, Polish Academy of Sciences; 2004. (vol 1).

Fauna Europaea [Internet]. 2013 [cited 2013 Aug 29]; Available from: http://www.faunaeur.org

Dafni A. Pollination ecology: a practical approach. Oxford: Oxford University Press; 1992.

Moore PD, Webb JA, Collinson ME. Pollen analysis. Oxford: Blackwell Scientific Publications; 1991.

Czarnecka B, Ptaszyńska A. Genetic diversity within the island population of Senecio macrophyllus M. Bieb. (Asteraceae), a vulnerable species in Poland. Scr Fac Rerum Nat Univ Ostrav. 2008;186:231–235.

Wild JD, Mayer E, Gottsberger G. Pollination and reproduction of Tussilago farfara (Asteraceae). Bot Jahrb. 2003;124(3):273–285. http://dx.doi.org/10.1127/0006-8152/2003/0124-0273

Castellanos MC, Wilson P, Keller SJ, Wolfe AD, Thomson JD. Anther evolution: pollen presentation strategies when pollinators differ. Am Nat. 2006;167(2):288–296. http://dx.doi.org/10.1086/498854

Denisow B. Pollen production of selected ruderal plant species in the Lublin area. Lublin: University of Life Sciences in Lublin Press; 2011.

Robertson AW, Lloyd DG. Rates of pollen deposition and removal in Myosotis colensoi. Func Ecol. 1993;7(5):549. http://dx.doi.org/10.2307/2390131

Sargent RD, Roitberg BD. Seasonal decline in male-phase duration in a protandrous plant: a response to increased mating opportunities? Func Ecol. 2000;14(4):484–489. http://dx.doi.org/10.1046/j.1365-2435.2000.00453.x

Harper JL, Wood WA. Senecio jacobaea L. J Ecol. 1957;45(2):617–637. http://dx.doi.org/10.2307/2256946

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

Shaffer ML. Minimum population sizes for species conservation. BioScience. 1981;31(2):131–134. http://dx.doi.org/10.2307/1308256

Frankel OH, Brown AND, Burdon JJ. The conservation of plant biodiversity. Cambridge: Cambridge University Press; 1995.

Czarnecka B. The effect of changes of xerothermic communities on the population fates of Senecio macrophyllus M. Bieb., a long-lived steppe plant (White Mountain, the Tomaszów Roztocze). In: Ratyńska H, Waldon B, editors. Xerothermic grasslands in Poland – the current state and perspectives of protection. Bydgoszcz: Kazimierz Wielki University in Bydgoszcz Press; 2010. p. 301–316.

Larsson M. Higher pollinator effectiveness by specialist than generalist flower-visitors of unspecialized Knautia arvensis (Dipsacaceae). Oecologia. 2005;146(3):394–403. http://dx.doi.org/10.1007/s00442-005-0217-y

Andersson S. Floral display and pollination success in Achillea ptarmica (Asteraceae). Ecography. 1991;14(3):186–191. http://dx.doi.org/10.1111/j.1600-0587.1991.tb00651.x

Douglas KL, Cruden RW. he 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

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

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/10.1111/j.1095-8312.2000.tb01221.x

Franzén M, Larsson M. Seed set differs in relation to pollen and nectar foraging flower visitors in an insect-pollinated herb. Nord J Bot. 2009;27(4):274–283. http://dx.doi.org/10.1111/j.1756-1051.2009.00348.x