Pollination biology of the urban populations of an ancient forest, spring ephemeral plant

Maciej A. Ziemiański, Marcin Zych

Abstract


Habitat fragmentation, caused by, among all, agriculture and urbanization, is one of the most important drivers of plant biodiversity decline worldwide. One of the signs of deteriorating zoogamous plant reproduction is pollen limitation, often associated with a decline in pollinator diversity and abundance. Various authors predict that the most vulnerable taxa are outbreeding plant species characterized by specialist pollination systems. We have, therefore, focused on self-incompatible Corydalis solida, an ancient forest, spring ephemeral plant, growing in three remnant urban populations in the city of Warsaw (Poland). Over two years, we checked for pollen limitation and recorded insect diversity and abundance for C. solida flowers. Our study populations composed of self-incompatible individuals were mainly visited by generalist pollinators, and produced more seeds when supplementally pollinated. Pollen limitation, however, was greater during 1 year with an early spring onset, when we observed a decline in floral visitors diversity and activity. This was probably an effect of phenological mismatch between plants and their pollinators, in this case, mostly social bees, i.e., over-wintered bumblebee queens and Apis mellifera. We conclude that for outbreeding zoogamous spring ephemerals, such as C. solida serviced by generalist pollinators, changing climatic conditions may override the effects of habitat fragmentation and influence their reproductive success.

Keywords


bees; Corydalis; forest remnants; pollen limitation; pollination; self-incompatibility; urbanization; Warsaw

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References


Grimm NB, Faeth SH, Golubiewski NE, Redman CL, Wu JG, Bai XM, et al. Global change and the ecology of cities. Science. 2008;319(5864):756–760. http://dx.doi.org/10.1126/science.1150195

Seto KC, Fragkias M, Guneralp B, Reilly MK. A meta-analysis of global urban land expansion. PLoS One. 2011;6(8):e23777. http://dx.doi.org/10.1371/journal.pone.0023777

Goddard MA, Dougill AJ, Benton TG. Scaling up from gardens: biodiversity conservation in urban environments. Trends Ecol Evol. 2010;25(2):90–98. http://dx.doi.org/10.1016/j.tree.2009.07.016

Magrach A, Laurance WF, Larrinaga AR, Santamaria L. Meta-analysis of the effects of forest fragmentation on interspecific interactions. Conserv Biol. 2014;28(5):1342–1348. http://dx.doi.org/10.1111/cobi.12304

Willmer P. Pollination and floral ecology. Princeton, NJ: Princeton University Press; 2011. http://dx.doi.org/10.1515/9781400838943

Knight TM, Steets JA, Vamosi JC, Mazer SJ, Burd M, Campbell DR, et al. Pollen limitation of plant reproduction: pattern and process. Ann Rev Ecol Evol Syst. 2005;36:467–497. http://dx.doi.org/10.1146/annurev.ecolsys.36.102403.115320

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

Newman BJ, Ladd P, Brundrett M, Dixon KW. Effects of habitat fragmentation on plant reproductive success and population viability at the landscape and habitat scale. Biol Conserv. 2013;159:16–23. http://dx.doi.org/10.1016/j.biocon.2012.10.009

Verboven HAF, Aertsen W, Brys R, Hermy M. Pollination and seed set of an obligatory outcrossing plant in an urban–peri-urban gradient. Perspect Plant Ecol Evol Syst. 2014;16(3):121–131. http://dx.doi.org/10.1016/j.ppees.2014.03.002

Eckert CG, Kalisz S, Geber MA, Sargent R, Elle E, Cheptou PO, et al. Plant mating systems in a changing world. Trends Ecol Evol. 2010;25(1):35–43. http://dx.doi.org/10.1016/j.tree.2009.06.013

Thomann M, Imbert E, Devaux C, Cheptou PO. Flowering plants under global pollinator decline. Trends Plant Sci. 2013;18(7):353–359. http://dx.doi.org/10.1016/j.tplants.2013.04.002

Richards AJ. Plant breeding systems. Oxford: Bios Scientific; 1997. http://dx.doi.org/10.1007/978-1-4899-3043-9

Myczko Ł, Banaszak-Cibicka W, Sparks T, Tryjanowski P. Do queens of bumblebee species differ in their choice of flower colour morphs of Corydalis cava (Fumariaceae)? Apidologie. 2015;46(3):337–345. http://dx.doi.org/10.1007/s13592-014-0326-x

Johnson SD, Steiner KE. Generalization versus specialization in plant pollination systems. Trends Ecol Evol. 2000;15(4):140–143. http://dx.doi.org/10.1016/S0169-5347(99)01811-X

Aizen MA, Ashworth L, Galetto L. Reproductive success in fragmented habitats: do compatibility systems and pollination specialization matter? J Veg Sci. 2002;13(6):885–892. http://dx.doi.org/10.1111/j.1654-1103.2002.tb02118.x

Corbet SA. A typology of pollination systems: implications for crop management and the conservation of wild plants. In: Waser NM, Ollerton J, editors. Plant-pollinator interactions from specialization to generalization. Chicago, IL: The University of Chicago Press; 2006. p. 315–340.

Aguilar R, Ashworth L, Galetto L, Aizen MA. Plant reproductive susceptibility to habitat fragmentation: review and synthesis through a meta-analysis. Ecol Lett. 2006;9(8):968–980. http://dx.doi.org/10.1111/j.1461-0248.2006.00927.x

Motten AF. Pollination ecology of the spring wildflower community of a temperate deciduous forest. Ecol Monogr. 1986;56(1):21–42. http://dx.doi.org/10.2307/2937269

Kudo G, Ida TY. Early onset of spring increases the phenological mismatch between plants and pollinators. Ecology. 2013;94(10):2311–2320. http://dx.doi.org/10.1890/12-2003.1

Hermy M, Honnay O, Firbank L, Grashof-Bokdam C, Lawesson JE. An ecological comparison between ancient and other forest plant species of Europe, and the implications for forest conservation. Biol Conserv. 1999;91(1):9–22. http://dx.doi.org/10.1016/s0006-3207(99)00045-2

Knuth P. Handbuch der Blütenbiologie, II Band, 1. Teil: Ranunculaceae bis Compostitae. Leipzig: Verlag von Wilhelm Engelman; 1898.

Fryxell PA. Mode of reproduction of higher plants. Bot Rev. 1957;23(3):135–233. http://dx.doi.org/10.1007/BF02869758

Sikorski P. Wpływ naturyzacji parku miejskiego na różnorodność florystyczną runa i trawników parkowych. Warsaw: Wieś Jutra Sp.z o.o.; 2013.

Denisow B, Strzałkowska-Abramek M, Bożek M, Jeżak A. Early spring nectar and pollen and insect visitor behavior in two Corydalis species (Papaveraceae). J Apic Sci. 2014;58(1):93–102. http://dx.doi.org/10.2478/jas-2014-0009

Zając EU. Papaveraceae. In: Jasiewicz A, editor. Dwuliścienne wolnopłatkowe – dwuokwia­towe. 2nd ed. Warszawa: Państwowe Wydawnictwo Naukowe; 1985. p. 102–126. (Flora Polska. Rośliny Naczyniowe; vol 4).

Kudo G, Maeda T, Narita K. Variation in floral sex allocation and reproductive success within inflorescences of Corydalis ambigua (Fumariaceae): pollination efficiency or resource limitation? J Ecol. 2001;89(1):48–56. http://dx.doi.org/10.1046/j.1365-2745.2001.00512.x

Maloof JE. Reproductive biology of a North American subalpine plant: Corydalis caseana A. Gray ssp. brandegei (S. Watson) G.B. Ownbey. Plant Species Biol. 2000;15(3):281–288. http://dx.doi.org/10.1111/j.1442-1984.2000.00047.x

Ohara M, Higashi S. Effects of inflorescence size on visits from pollinators and seed set of Corydalis ambigua (Papaveraceae). Oecologia. 1994;98(1):25–30. http://dx.doi.org/10.1007/bf00326086

Luoto M, Kuussaari M, Rita H, Salminen J, von Bonsdorff T. Determinants of distribution and abundance in the clouded Apollo butterfly: a landscape ecological approach. Ecography. 2001;24(5):601–617. http://dx.doi.org/10.1034/j.1600-0587.2001.d01-215.x

Ehlers BK. Geographic variation for elaiosome-seed size ratio and its allometric relationship in two closely related Corydalis species. Plant Ecol Divers. 2012;5(3):395–401. http://dx.doi.org/10.1080/17550874.2012.695812

Czerwińska-Jędrusiak B. Ludność i powierzchnia Warszawy w latach 1921–2008. Warsaw: Urząd Statystyczny w Warszawie; 2009.

Sikorski P, Borowski J, Sikorska D, Wierzba D, Kehl J, Włodarczyk S. Mało znane parki i zieleńce Warszawy jako rezerwuar dzikiej przyrody. In: Obidziński A, editor. Z Mazowsza na Polesie i Wileńszczyznę Zróżnicowanie i ochrona szaty roślinnej pogranicza Europy Środkowej i Północno-Wschodniej. Warsaw: Polish Botanical Society; 2010. p. 103–117.

Werblan-Jakubiec H, Zych M. University of Warsaw Botanic Garden. A guidebook. Warsaw: Muza SA; 2013.

Solińska-Górnicka B, Symonides E. Effect of a large city on the structure of coenoelements in a natural woodland in Warsaw. Vegetatio. 1990;88:163–176. http://dx.doi.org/10.1007/BF00044833

Elzinga CL, Salzer DW, Willoughby JW. Measuring and monitoring plant populations. Denver, CO: USDI Bureau of Land Management; 1998.

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

Bogdanowicz W, Chudzicka E, Pilipiuk I, Skibińska E. Fauna of Poland. Characteristics and checklist of species. Warsaw: Museum and Institute of Zoology, Polish Academy of Sciences; 2007.

Larson BMH, Barrett SCH. A comparative analysis of pollen limitation in flowering plants. Biol J Linn Soc Lond. 2000;69(4):503–520. http://dx.doi.org/10.1111/j.1095-8312.2000.tb01221.x

Bolker BM, Brooks ME, Clark CJ, Geange SW, Poulsen JR, Stevens MHH, et al. Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol. 2009;24(3):127–135. http://dx.doi.org/10.1016/j.tree.2008.10.008

Burd M. Bateman’s principle and plant reproduction: the role of pollen limitation in fruit and seed ste. Bot Rev. 1994;60:83–139. http://dx.doi.org/10.1007/BF02856594

Ashman TL, Knight TM, Steets JA, Amarasekare P, Burd M, Campbell DR, et al. Pollen limitation of plant reproduction: ecological and evolutionary causes and consequences. Ecology. 2004;85(9):2408–2421. http://dx.doi.org/10.1890/03-8024

Kudo G, Nishikawa Y, Kasagi T, Kosuge S. Does seed production of spring ephemerals decrease when spring comes early? Ecol Res. 2004;19(2):255–259. http://dx.doi.org/10.1111/j.1440-1703.2003.00630.x

Diekmann M. Relationship between flowering phenology of perennial herbs and meteorological data in deciduous forests of Sweden. Can J Bot. 1996;74(4):528–537. http://dx.doi.org/10.1139/b96-067

Fitter AH, Fitter RSR, Harris ITB, Williamson MH. Relationships between first flowering date and temperature in the flora of a locality in central England. Funct Ecol. 1995;9(1):55–60. http://dx.doi.org/10.2307/2390090

Thórhallsdóttir TE. Flowering phenology in the central highland of Iceland and implications for climatic warming in the Arctic. Oecologia. 1998;114(1):43–49. http://dx.doi.org/10.1007/s004420050418

Alford DV. A study of the hibernation of bumblebees (Hymenoptera: Bombidae) in southern England. J Anim Ecol. 1969;38(1):149–170. http://dx.doi.org/10.2307/2743

Macior LW. Pollination ecology of vernal angiosperms. Oikos. 1978;30(3):452–460. http://dx.doi.org/10.2307/3543340

Kudo G. Vulnerability of phenological synchrony between plants and pollinators in an alpine ecosystem. Ecol Res. 2014;29(4):571–581. http://dx.doi.org/10.1007/s11284-013-1108-z

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. 2012;14:285–294. http://dx.doi.org/10.1111/j.1438-8677.2011.00510.x

Zych M, Goldstein J, Roguz K, Stpiczynska M. The most effective pollinator revisited: pollen dynamics in a spring-flowering herb. Arthropod Plant Interact. 2013;7(3):315–322. http://dx.doi.org/10.1007/s11829-013-9246-3

Sparks TH, Langowska A, Głazaczow A, Wilkaniec Z, Bieńkowska M, Tryjanowski P. Advances in the timing of spring cleaning by the honeybee Apis mellifera in Poland. Ecol Entomol. 2010;35(6):788–791. http://dx.doi.org/10.1111/j.1365-2311.2010.01226.x

Higashi S, Ohara M, Arai H, Matsuo K. Robber-like pollinators – overwintered queen bumblebees foraging on Corydalis ambigua. Ecol Entomol. 1988;13(4):411–418. http://dx.doi.org/10.1111/j.1365-2311.1988.tb00373.x

Maloof JE. The effects of a bumble bee nectar robber on plant reproductive success and pollinator behavior. Am J Bot. 2001;88(11):1960–1965. http://dx.doi.org/10.2307/3558423

Kudo G, Ida TY. Carbon source for reproduction in a spring ephemeral herb, Corydalis ambigua (Papaveraceae). Funct Ecol. 2010;24(1):62–69. http://dx.doi.org/10.1111/j.1365-2435.2009.01601.x

Fenster CB, Armbruster WS, Wilson P, Dudash MR, Thomson JD. Pollination syndromes and floral specialization. Annu Rev Ecol Evol Syst. 2004;35:375–403. http://dx.doi.org/10.1146/annurev.ecolsys.34.011802.132347

Ollerton J, Killick A, Lamborn E, Watts S, Whiston M. Multiple meanings and modes: on the many ways to be a generalist flower. Taxon. 2007;56(3):717–728. http://dx.doi.org/10.2307/25065856

Bates AJ, Sadler JP, Fairbrass AJ, Falk SJ, Hale JD, Matthews TJ. Changing bee and hoverfly pollinator assemblages along an urban-rural gradient. PLoS One. 2011;6(8):e23459. http://dx.doi.org/10.1371/journal.pone.0023459

Hennig E, Ghazoul J. Pollinating animals in the urban environment. Urban Ecosyst. 2012;15:149–166. http://dx.doi.org/10.1007/s11252-011-0202-7

Jędrzejewska-Szmek K, Zych M. Flower-visitor and pollen transport networks in a large city: structure and properties. Arthropod Plant Interact. 2013;7(5):503–516. http://dx.doi.org/10.1007/s11829-013-9274-z

Banaszak-Cibicka W, Żmihorski M. Wild bees along an urban gradient: winners and losers. J Insect Conserv. 2012;16(3):331–343. http://dx.doi.org/10.1007/s10841-011-9419-2

Geslin B, Gauzens B, Thébault E, Dajoz I. Plant-pollinator networks along a gradient of urbanisation. PLoS One. 2013;8(5):e63421. http://dx.doi.org/10.1371/journal.pone.0063421

Bascompte J, Jordano P, Melian CJ, Olesen JM. The nested assembly of plant-animal mutualistic networks. Proc Natl Acad Sci USA. 2003;100(16):9383–9387. http://dx.doi.org/10.1073/pnas.1633576100

Bascompte J, Jordano P, Olesen JM. Asymmetric coevolutionary networks facilitate biodiversity maintenance. Science. 2006;312(5772):431–433. http://dx.doi.org/10.1126/science.1123412

Stang M, Klinkhamer PGL, van der Meijden E. Asymmetric specialization and extinction risk in plant-flower visitor webs: a matter of morphology or abundance? Oecologia. 2007;151(3):442–453. http://dx.doi.org/10.1007/s00442-006-0585-y

Ashworth L, Aguilar R, Galetto L, Aizen MA. Why do pollination generalist and specialist plant species show similar reproductive susceptibility to habitat fragmentation? J Ecol. 2004;92(4):717–719. http://dx.doi.org/10.1111/j.0022-0477.2004.00910.x

Verboven HAF, Brys R, Hermy M. Sex in the city: reproductive success of Digitalis purpurea in a gradient from urban to rural sites. Landsc Urban Plan. 2012;106(2):158–164. http://dx.doi.org/10.1016/j.landurbplan.2012.02.015

Pellissier V, Muratet A, Verfaillie F, Machon N. Pollination success of Lotus corniculatus (L.) in an urban context. Acta Oecol (Montrouge). 2012;39:94–100. http://dx.doi.org/10.1016/j.actao.2012.01.008

Wee AKS, Low SY, Webb EL. Pollen limitation affects reproductive outcome in the bird-pollinated mangrove Bruguiera gymnorrhiza (Lam.) in a highly urbanized environment. Aquat Bot. 2015;120:240–243. http://dx.doi.org/10.1016/j.aquabot.2014.09.001

Williams NM, Winfree R. Local habitat characteristics but not landscape urbanization drive pollinator visitation and native plant pollination in forest remnants. Biol Conserv. 2013;160:10–18. http://dx.doi.org/10.1016/j.biocon.2012.12.035

Moore LJ, Kosut M. Buzz: urban beekeeping and the power of the bee. New York, NY: New York University Press; 2013.

Central Statistical Office. Statistical Bulletin. Warsaw: Central Statistical Office; 2012.

Central Statistical Office. Statistical Bulletin. Warsaw: Central Statistical Office; 2013.

Central Statistical Office. Statistical Bulletin. Warsaw: Central Statistical Office; 2014.




DOI: https://doi.org/10.5586/asbp.3489

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