FLOWERING PHENOLOGY AND POLLEN PRODUCTION OF THREE EARLY SPRING Pulsatilla SPECIES
Monika Strzałkowska-Abramek
University of Life Sciences, Lublin, PolandJacek Jachuła
University of Life Sciences, Lublin, PolandMarta Dmitruk
University of Life Sciences, Lublin, PolandElżbieta Pogroszewska
University of Life Sciences, Lublin, PolandAbstract
Blooming biology and pollen production of the following species: Pulsatilla zimmermannii Soó, P. halleri (All.) Willd., and P. vulgaris Mill. grown in UMCS Botanical Garden in Lublin, Poland (51°16'N, 22°30'E) was studied. The species attract insect visitors with large (size 6–8 cm in diameter), colourful, campanulate, actinomorphic flowers. The androecium is multistaminate (min–max: 142–282 anthers per flower), spirally arranged. Minute droplets of nectar were noted at the base of androecium and on stami-nodes. The anthers dehisced subsequently and pollen of a single flower was available to insects for 5–11 (7) days. On average, P. zimmermannii was found to produce the highest amount of pollen (9.16 g per 1 m2), which was 2 times more pollen than P. vulgaris (4.22 g per 1 m2), while P. halleri produced 7.63 g per 1 m2. Pollen grains of the Pulsatilla species are medium in size (P axis ranged 29.8–38.4 μm, and E axis ranged 32.3–39.6 μm) and are oblate-spheroid in shape (P/E index ranged between 0.90 and 0.95). If planted together, the species will provide pollen from first days of April until end of the month, i.e. during the period when seasonal activity of Apoidea insects begins. Pulsatilla species might contribute to lists of garden plants that attract insect visitors with abundant pollen reward and minute nectar.
Keywords:
flowering, staminodes, pollen output, pollen shape, Pulsatilla spp.References
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Colding, J., Lundberg, J., Folke, C. (2006). Incorporating green-area user groups in urban ecosystem management. AMBIO: J. Hum. Environ., 35(5), 237–244. doi: 10.1579/05-A-098R.1
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Gallai, N. (2008). Array for the economic valuation of the contribution of insect pollination to agriculture and impact on the welfare. In: FAOSTAT [Internet]. Available: http://www.internationalpollinatorsinitiative.org/uploads/POLLINATIONVALUEARRAY.xls Garbuzov, M., Ratnieks, F.L.W. (2014). Quantifying variation among garden plants in attractive-ness to bees and other flower-visiting insects. Funct. Ecol., 28(2), 364–374. doi: 10.1111/1365-2435.12178
Goulson, D., Nicholls, E., Botías, C., Rotheray, E.L. (2015). Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science, 347(6229), 1255957. doi: 10.1126/science.1255957
Grabowska, B., Kubala, T. (2012). Encyklopedia bylin. Zysk i S-ka, Poznań.
Grzyl, A., Biedrzyński, M., Zielińska, K.M., Rewicz, A. (2014). The relationship between climat-ic conditions and generative reproduction of a lowland population of Pulsatilla vernalis: the last breath of a relict plant or a fluctuating cycle of regeneration? Plant. Ecol., 215(4), 457–466.
Hashani, Z., Shuka, L. (2013). Pulsatilla halleri (All.) Willd. and Viola schariensis Erben, New species for the flora of Kosovo. Nat. Montenegro, 12(4), 569–574.
Hicks, D.M., Ouvrard, P., Baldock, K.C., Baude, M., Goddard, M.A., Kunin, W.E., et al. (2016). Food for pollinators: quantifying the nectar and pollen resources of urban flower meadows. PloS one, 11(6), e0158117. doi: 10.1371/journal.pone.0158117
Huang, S.-Q., Takahashi, Y., Dafni, A. (2002). Why does the flower stalk of Pulsatilla cernua (Ranunculaceae) bend during anthesis? Am. J. Bot., 89(10), 1599–1603. doi:10.3732/ajb.89.10.1599
Jabłoński, B. (2002). Notes on the method to investigate nectar secretion rate in flowers. J. Apic. Sci., 46(2), 117–125.
Jensen, U., Kadereit, J.W. (2012). Systematics and Evolution of the Ranunculiflorae. Springer Sci. & Business Media
Kugler, H. (1970). Blütenökologie. Gustav Fischer Verlag, Stuttgart.
Kumova, U., Korkmaz, A. (2013). The research on determination of flowering phenology of phacelia (Phacelia tanacetifolia Bentham) and its nectar and pollen potential. Mellifera, 13(25), 30–40.
Mártonfiová, L. (2004). Karyotype studies in Pulsatilla zimmermanni. Biologia (Bratisl), 59(1), 61–64.
Mirek, Z., Piekos-Mirkowa, H., Zając, A., Zając, M. (2002). Flowering plants and pteridophytes of Poland. A checklist. W. Szafer Institute of Botany, PAN, Kraków.
Pacini, E. (2000). From anther and pollen ripening to pollen presentation. Plant. Syst. Evol. 222, 19–43. doi: 10.1007/BF00984094
Pilt, I., Kukk, U. (2002). Pulsatilla patens and Pulsatilla pratensis (Ranunculaceae) in Estonia: distribution and ecology. Proc. Estonian Acad. Sci. Biol. Ecol., 51(4), 242–256.
Potts, S.G., Biesmeijer, J.C., Kremen, C., Neumann, P., Schweiger, O., Kunin, W.E. (2010). Global pollinator declines: trends, impacts and drivers. Trends Ecol. Evol., 25(6), 345–353. doi: 10.1016/j.tree.2010.01.007
Šaulienė, I., Brinkyte, E. (2009). The impact of phytohormones on pasqueflower (Pulsatilla) regeneration in vitro. Acta Biol. Univ. Daugavpiliensis, 9(2), 249–254.
Sirohi, M.H., Jackson, J., Edwards, M., Ollerton, J. (2015). Diversity and abundance of solitary and primitively eusocial bees in an urban centre: a case study from Northampton (England). J. Insect Conserv., 19(3), 487–500. doi: 10.1007/s10841-015-9769-2
Stanisz, A. (2007). Przystępny kurs statystyki z zastosowaniem Statistica na przykładach z medycyny. Statsoft Polska. Kraków. 359 pp.
Strzałkowska-Abramek, M., Tymoszuk, K., Jachuła, J., Bożek, M. (2016). Nectar and pollen production in Arabis procurrens Waldst. & Kit. and Iberis sempervirens L. (Brassicaceae). Acta Agrobot., 69(1). doi: 10.5586/aa.1656
Szczecińska, M., Sawicki, J. (2015). Genomic resources of three Pulsatilla species reveal evolutionary hotspots, species-specific sites and variable plastid structure in the family Ranunculaceae. Int. J. Mol. Sci., 16(9), 22258–22279. doi: 10.3390/ijms160922258
Szklanowska, K. (1995). Pollen flows of crowfoot family (Ranunculaceae L.) from some natural plant communities. Changes in fauna of wild bees in Europe. Pedagog. Univ. Bydgoszcz, 201–209.
Thomann, M., Imbert, E., Devaux, C., Cheptou, P.O. (2013). Flowering plants under global pollinator decline. Trends Plant Sci., 18(7), 353–359. doi: 10.1016/j.tplants.2013.04.002
Torvik, S.E., Borgen, L., Berg, R.Y. (1998). Aspects of reproduction in Pulsatilla pratensis in Norway. Nord. J. Bot., 18(4), 385–391. doi: 10.1111/j.1756-1051.1998.tb01515.x Turner, R.G. (2005). Botanica: the illustrated A-Z of over 10,000 garden plants and how to cultivate them. Könemann Tandem Verlag GmbH, Königswinter.
Turrini, T., Knop, E. (2015). A landscape ecology approach identifies important drivers of urban biodiversity. Glob. Chang Biol., 21, 1652–1667. doi: 10.1111/gcb.12825
Vanbergen, A.J. (2013). Threats to an ecosystem service: pressures on pollinators. Front. Ecol. Environ., 11(5), 251–259. doi: 10.1890/120126
Walker, K.J., Pinches, C.E. (2011). Reduced grazing and the decline of Pulsatilla vulgaris Mill. (Ranunculaceae) in England, UK. Biol. Cons., 144(12), 3098–3105.
Weryszko-Chmielewska, E., Sulborska, A. (2011). Staminodial nectary structure in two Pulsatilla (L.) species. Acta Biol. Cracov. Ser. Bot., 53(2), 94–103.
Wrzesień, M., Denisow, B. (2006). The share of nectariferous and polleniferous taxons in chosen patches of thermophilous grasslands of the Lublin Upland. Acta Agrobot., 59(1). doi: 10.5586/aa.2006.021
Wrzesień, M., Jachuła, J., Denisow, B. (2016). Railway embankments – refuge areas for food flora and pollinators in agricultural landscape. J. Apic. Sci., 60(1), 39–51. doi: 10.1515/JAS- -2016-0004
Ziembińska-Tworzydło, M., Kohlman-Adamska, A. (2003). Morfologia. In: Palinologia Dybova-Jachovicz, S., Sadowska, A. Instytut Botaniki PAN, Kraków.
Bożek, M., Strzałkowska-Abramek, M., Denisow, B. (2015). Nectar and pollen production and insect visitation on ornamentals from the genus Hosta Tratt. (Asparagaceae). J. Apic. Sci., 59(2), 115–125. doi: 10.1515/jas-2015-0021
Carvalheiro, L.G., Biesmeijer, J.C., Benadi, G., Fründ, J., Stang, M., Bartomeus, I., et al. (2014). The potential for indirect effects between co-flowering plants via shared pollinators depends on resource abundance, accessibility and relatedness. Ecol. Lett., 17(11), 1389–1399. doi: 10.1111/ele.12342 Chittka, L., Thomson, J.D., Waser, N.M. (1999). Flower constancy, insect psychology, and plant evolution. Naturwissenschaften, 86(8), 361–377. doi: 10.1007/s001140050636
Colding, J., Lundberg, J., Folke, C. (2006). Incorporating green-area user groups in urban ecosystem management. AMBIO: J. Hum. Environ., 35(5), 237–244. doi: 10.1579/05-A-098R.1
Czarnecka, B., Denisow, B. (2014). Floral biology of Senecio macrophyllus M. Bieb. (Asteraceae), a rare Central European steppe plant. Acta Soc. Bot. Pol., 83(1), 29–37. http://dx.doi.org/10.5586/asbp.2014.002
Denisow, B., Bożek, M. (2006). Blooming biology and pollen abundance of Anemone japonica Houtt. = Anemone × hybrida hort. Acta Agrobot., 59(1), 139–146. doi: 10.5586/aa.2006.014
Denisow, B., Wrzesień, M. (2006). The study of blooming and pollen efficiency of Adonis vernalis L. in xerothermic plant communities. J. Apic. Sci., 50(1), 25–32.
Denisow, B., Bożek, M. (2008). Blooming and pollen production of two Lamium L. species. J. Apic. Sci., 52(1), 21–30.
Denisow, B., Wrzesień, M. (2015 a). The importance of field-margin location for maintenance of food niches for pollinators. J. Apic. Sci., 59(1), 27–37. doi: 10.1515/jas -2015-0002
Denisow, B., Wrzesień, M. (2015 b). Does vegetation impact on the population dynamics and male function in Anemone sylvestris L. (Ranunculaceae)? A case study in three natural popu-lations of xerothermic grasslands. Acta Soc. Bot. Pol., 84(2), 197–205. doi: 10.5586/asbp.2015.017
Denisow, B., Strzałkowska-Abramek, M., Bożek, M., Jeżak, A. (2014 a). Ornamental representa-tives of the genus Centaurea L. as a pollen source for bee friendly gardens. J. Apic. Sci., 58(2), 49–58. doi: 10.2478/JAS-2014-0016
Denisow, B., Strzałkowska-Abramek, M., Bożek, M., Jeżak, A. (2014 b). Early spring nectar and pollen and insect visitor behavior in two Corydalis species (Papaveraceae). J. Apic. Sci. 58(1), 93–102. doi: 10.2478/jas-2014-0009
Denisow, B., Wrzesień, M., Cwener, A. (2014). Pollination and floral biology of Adonis vernalis L. (Ranunculaceae) – a case study of threatened species. Acta Soc. Bot. Pol., 83(1), 29–37. doi: 10.5586/asbp.2014.001
Denisow, B., Pogroszewska, E., Laskowska, H. (2015). The effect of silicon on nectar and pollen production in Hosta Tratt. ‘Krossa Regal’ Acta Sci. Pol. Hortorum Cultus, 14(4), 131–142.
Denisow, B., Antoń, S., Wrzesień, M. (2016). Morphology of Anemone sylvestris L. flower (Ranunculaceae). Acta Bot. Croat., 75(1), 74–80. doi: 10.1515/botcro-2016-0009 Dicks, L.V., Baude, M., Roberts, S.P., Phillips, J., Green, M., Carvell, C. (2015). How much flower-rich habitat is enough for wild pollinators? Answering a key policy question with in-complete knowledge. Ecol. Entomol., 40(S1), 22–35. doi: 10.1111/een.12226
Erdtman, G. (1954) An introduction to pollen analysis. Waltham, Mass., USA. 239 pp.
Fussell, M., Corbet, S.A. (1992). Flower usage by bumble-bees: a basis for forage plant management. J. Appl. Ecol., 29(2), 451–465. doi: 10.2307/2404513
Gallai, N. (2008). Array for the economic valuation of the contribution of insect pollination to agriculture and impact on the welfare. In: FAOSTAT [Internet]. Available: http://www.internationalpollinatorsinitiative.org/uploads/POLLINATIONVALUEARRAY.xls Garbuzov, M., Ratnieks, F.L.W. (2014). Quantifying variation among garden plants in attractive-ness to bees and other flower-visiting insects. Funct. Ecol., 28(2), 364–374. doi: 10.1111/1365-2435.12178
Goulson, D., Nicholls, E., Botías, C., Rotheray, E.L. (2015). Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science, 347(6229), 1255957. doi: 10.1126/science.1255957
Grabowska, B., Kubala, T. (2012). Encyklopedia bylin. Zysk i S-ka, Poznań.
Grzyl, A., Biedrzyński, M., Zielińska, K.M., Rewicz, A. (2014). The relationship between climat-ic conditions and generative reproduction of a lowland population of Pulsatilla vernalis: the last breath of a relict plant or a fluctuating cycle of regeneration? Plant. Ecol., 215(4), 457–466.
Hashani, Z., Shuka, L. (2013). Pulsatilla halleri (All.) Willd. and Viola schariensis Erben, New species for the flora of Kosovo. Nat. Montenegro, 12(4), 569–574.
Hicks, D.M., Ouvrard, P., Baldock, K.C., Baude, M., Goddard, M.A., Kunin, W.E., et al. (2016). Food for pollinators: quantifying the nectar and pollen resources of urban flower meadows. PloS one, 11(6), e0158117. doi: 10.1371/journal.pone.0158117
Huang, S.-Q., Takahashi, Y., Dafni, A. (2002). Why does the flower stalk of Pulsatilla cernua (Ranunculaceae) bend during anthesis? Am. J. Bot., 89(10), 1599–1603. doi:10.3732/ajb.89.10.1599
Jabłoński, B. (2002). Notes on the method to investigate nectar secretion rate in flowers. J. Apic. Sci., 46(2), 117–125.
Jensen, U., Kadereit, J.W. (2012). Systematics and Evolution of the Ranunculiflorae. Springer Sci. & Business Media
Kugler, H. (1970). Blütenökologie. Gustav Fischer Verlag, Stuttgart.
Kumova, U., Korkmaz, A. (2013). The research on determination of flowering phenology of phacelia (Phacelia tanacetifolia Bentham) and its nectar and pollen potential. Mellifera, 13(25), 30–40.
Mártonfiová, L. (2004). Karyotype studies in Pulsatilla zimmermanni. Biologia (Bratisl), 59(1), 61–64.
Mirek, Z., Piekos-Mirkowa, H., Zając, A., Zając, M. (2002). Flowering plants and pteridophytes of Poland. A checklist. W. Szafer Institute of Botany, PAN, Kraków.
Pacini, E. (2000). From anther and pollen ripening to pollen presentation. Plant. Syst. Evol. 222, 19–43. doi: 10.1007/BF00984094
Pilt, I., Kukk, U. (2002). Pulsatilla patens and Pulsatilla pratensis (Ranunculaceae) in Estonia: distribution and ecology. Proc. Estonian Acad. Sci. Biol. Ecol., 51(4), 242–256.
Potts, S.G., Biesmeijer, J.C., Kremen, C., Neumann, P., Schweiger, O., Kunin, W.E. (2010). Global pollinator declines: trends, impacts and drivers. Trends Ecol. Evol., 25(6), 345–353. doi: 10.1016/j.tree.2010.01.007
Šaulienė, I., Brinkyte, E. (2009). The impact of phytohormones on pasqueflower (Pulsatilla) regeneration in vitro. Acta Biol. Univ. Daugavpiliensis, 9(2), 249–254.
Sirohi, M.H., Jackson, J., Edwards, M., Ollerton, J. (2015). Diversity and abundance of solitary and primitively eusocial bees in an urban centre: a case study from Northampton (England). J. Insect Conserv., 19(3), 487–500. doi: 10.1007/s10841-015-9769-2
Stanisz, A. (2007). Przystępny kurs statystyki z zastosowaniem Statistica na przykładach z medycyny. Statsoft Polska. Kraków. 359 pp.
Strzałkowska-Abramek, M., Tymoszuk, K., Jachuła, J., Bożek, M. (2016). Nectar and pollen production in Arabis procurrens Waldst. & Kit. and Iberis sempervirens L. (Brassicaceae). Acta Agrobot., 69(1). doi: 10.5586/aa.1656
Szczecińska, M., Sawicki, J. (2015). Genomic resources of three Pulsatilla species reveal evolutionary hotspots, species-specific sites and variable plastid structure in the family Ranunculaceae. Int. J. Mol. Sci., 16(9), 22258–22279. doi: 10.3390/ijms160922258
Szklanowska, K. (1995). Pollen flows of crowfoot family (Ranunculaceae L.) from some natural plant communities. Changes in fauna of wild bees in Europe. Pedagog. Univ. Bydgoszcz, 201–209.
Thomann, M., Imbert, E., Devaux, C., Cheptou, P.O. (2013). Flowering plants under global pollinator decline. Trends Plant Sci., 18(7), 353–359. doi: 10.1016/j.tplants.2013.04.002
Torvik, S.E., Borgen, L., Berg, R.Y. (1998). Aspects of reproduction in Pulsatilla pratensis in Norway. Nord. J. Bot., 18(4), 385–391. doi: 10.1111/j.1756-1051.1998.tb01515.x Turner, R.G. (2005). Botanica: the illustrated A-Z of over 10,000 garden plants and how to cultivate them. Könemann Tandem Verlag GmbH, Königswinter.
Turrini, T., Knop, E. (2015). A landscape ecology approach identifies important drivers of urban biodiversity. Glob. Chang Biol., 21, 1652–1667. doi: 10.1111/gcb.12825
Vanbergen, A.J. (2013). Threats to an ecosystem service: pressures on pollinators. Front. Ecol. Environ., 11(5), 251–259. doi: 10.1890/120126
Walker, K.J., Pinches, C.E. (2011). Reduced grazing and the decline of Pulsatilla vulgaris Mill. (Ranunculaceae) in England, UK. Biol. Cons., 144(12), 3098–3105.
Weryszko-Chmielewska, E., Sulborska, A. (2011). Staminodial nectary structure in two Pulsatilla (L.) species. Acta Biol. Cracov. Ser. Bot., 53(2), 94–103.
Wrzesień, M., Denisow, B. (2006). The share of nectariferous and polleniferous taxons in chosen patches of thermophilous grasslands of the Lublin Upland. Acta Agrobot., 59(1). doi: 10.5586/aa.2006.021
Wrzesień, M., Jachuła, J., Denisow, B. (2016). Railway embankments – refuge areas for food flora and pollinators in agricultural landscape. J. Apic. Sci., 60(1), 39–51. doi: 10.1515/JAS- -2016-0004
Ziembińska-Tworzydło, M., Kohlman-Adamska, A. (2003). Morfologia. In: Palinologia Dybova-Jachovicz, S., Sadowska, A. Instytut Botaniki PAN, Kraków.
Monika Strzałkowska-Abramek
University of Life Sciences, Lublin, Poland
University of Life Sciences, Lublin, Poland
Jacek Jachuła
University of Life Sciences, Lublin, Poland
University of Life Sciences, Lublin, Poland
Marta Dmitruk
University of Life Sciences, Lublin, Poland
University of Life Sciences, Lublin, Poland
Elżbieta Pogroszewska
University of Life Sciences, Lublin, Poland
University of Life Sciences, Lublin, Poland
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