Changes in environmental conditions are likely to have a complex effect on the growth of plants, their phenology, plant-pollinator interactions, and reproductive success. The current world is facing an ongoing climate change along with other human-induced environmental changes. Most research has focused on the impact of increasing temperature as a major driving force for climate change, but other factors may have important impacts on plant traits and pollination too and these effects may vary from season to season. In addition, it is likely that the effects of multiple environmental factors, such as increasing temperature, water availability, and nitrogen enrichment are not independent. Therefore, we tested the impact of two key factors-water, and nitrogen supply-on plant traits, pollination, and seed production in Sinapis alba (Brassicaceae) in three seasons defined as three temperature conditions with two levels of water and nitrogen supply in a factorial design. We collected data on multiple vegetative and floral traits and assessed the response of pollinators in the field. Additionally, we evaluated the effect of growing conditions on seed set in plants exposed to pollinators and in hand-pollinated plants. Our results show that water stress impaired vegetative growth, decreased flower production, and reduced visitation by pollinators and seed set, while high amount of nitrogen increased nectar production under low water availability in plants grown in the spring. Temperature modulated the effect of water and nitrogen availability on vegetative and floral traits and strongly affected flowering phenology and flower production. We demonstrated that changes in water and nitrogen availability alter plant vegetative and floral traits, which impacts flower visitation and consequently plant reproduction. We conclude that ongoing environmental changes such as increasing temperature, altered precipitation regimes and nitrogen enrichment may thus affect plant-pollinator interactions with negative consequences for the reproduction of wild plants and insect-pollinated crops.

Department of Zoology Faculty of Science University of South Bohemia České Budějovice Czech Republic

Institute of Entomology Biology Centre of the Czech Academy of Sciences České Budějovice Czech Republic

Zobrazit více v PubMed

Akter A, Biella P, Klecka J. Effects of small-scale clustering of flowers on pollinator foraging behaviour and flower visitation rate. PLOS ONE. 2017;12(11):e0187976. doi: 10.1371/journal.pone.0187976. PubMed DOI PMC

Baker HG, Baker I. Floral nectar sugar constituents in relation to pollinator type. In: Jones CE, Little RJ, editors. Handbook of experimental pollination biology. Van Nostrand Reinhold; New York: 1983. pp. 117–141.

Barnabás B, Jäger K, Fehér A. The effect of drought and heat stress on reproductive processes in cereals. Plant Cell and Environment. 2008;31(1):11–38. PubMed

Bartomeus I, Ascher JS, Wagner D, Danforth BN, Colla S, Kornbluth S, Winfree R. Climate-associated phenological advances in bee pollinators and bee-pollinated plants. Proceedings of the National Academy of Sciences of the United States of America. 2011;108(51):20645–20649. doi: 10.1073/pnas.1115559108. PubMed DOI PMC

Basnett S, Ganesan R, Devy SM. Floral traits determine pollinator visitation in Rhododendron species across an elevation gradient in the Sikkim Himalaya. Alpine Botany. 2019;129:81–94. doi: 10.1007/s00035-019-00225-3. DOI

Battye W, Aneja VP, Schlesinger WH. Is nitrogen the next carbon? Earth’s Future. 2017;5(9):894–904. doi: 10.1002/2017EF000592. DOI

Behboudian MH, Ma Q, Turner NC, Palta JA. Reactions of chickpea to water stress: yield and seed composition. Journal of the Science of Food and Agriculture. 2001;81(13):1288–1291. doi: 10.1002/jsfa.939. DOI

Bernal M, Estiarte M, Peñuelas J. Drought advances spring growth phenology of the Mediterranean shrub Erica multiflora. Plant Biology. 2011;13:252–257. doi: 10.1111/j.1438-8677.2010.00358.x. PubMed DOI

Biella P, Akter A, Ollerton J, Tarrant S, Janeček Š, Jersáková J, Klecka J. Experimental loss of generalist plants reveals alterations in plant–pollinator interactions and a constrained flexibility of foraging. Scientific Reports. 2019;9:7376. doi: 10.1038/s41598-019-43553-4. PubMed DOI PMC

Blum A. Crop responses to drought and the interpretation of adaptation. Plant Growth Regulation. 1996;20:135–148. doi: 10.1007/BF00024010. DOI

Bobbink R, Hicks K, Galloway J, et al. Global assessment of nitrogen deposition effects on terrestrial plant diversity: a synthesis. Ecological Applications. 2010;20(1):30–59. doi: 10.1890/08-1140.1. PubMed DOI

Brown J, Davis JB, Esser A. Pacific Northwest condiment yellow mustard (Sinapis alba L.) grower guide. Subcontract report - National Renewable Energy Laboratory. University of Idahohttp://www.nrel.gov/docs/fy05osti/36307.pdf 2005

Burkle L, Irwin RE. The importance of interannual variation and bottom–up nitrogen enrichment for plant–pollinator networks. Oikos. 2009;118:1816–1829. doi: 10.1111/j.1600-0706.2009.17740.x. DOI

Burkle LA, Irwin RE. Beyond biomass: measuring the effects of community-level nitrogen enrichment on floral traits, pollinator visitation and plant reproduction. Journal of Ecology. 2010;98:705–717. doi: 10.1111/j.1365-2745.2010.01648.x. DOI

Carroll AB, Pallardy SG, Galen C. Drought stress, plant water status, and floral trait expression in fireweed, Epilobium angustifolium (Onagraceae) American Journal of Botany. 2001;88:438–446. doi: 10.2307/2657108. PubMed DOI

Carromero W, Hamrick JL. The mating system of Verbascum thapsus (Scrophulariaceae): the effect of plant height. International Journal of Plant Sciences. 2005;166:979–983. doi: 10.1086/449315. DOI

Christensen JH, Carter TR, Rummukainen M, Amanatidis G. Evaluating the performance and utility of regional climate models: the PRUDENCE project. Climatic Change. 2007;81:1–6.

Conner JK, Rush S. Effects of flower size and number on pollinator visitation to wild radish, Raphanus raphanistrum. Oecologia. 1996;105(4):509–516. doi: 10.1007/BF00330014. PubMed DOI

Corbet SA, Fussell M, Ake R, Fraser A, Gunson C, Savage A, Smith K. Temperature and the pollinating activity of social bees. Ecological Entomology. 1993;18:17–30. doi: 10.1111/j.1365-2311.1993.tb01075.x. DOI

Cossani CM, Slafer GA, Savin R. Nitrogen and water use efficiencies of wheat and barley under a Mediterranean environment in Catalonia. Field Crops Research. 2012;128:109–118. doi: 10.1016/j.fcr.2012.01.001. DOI

Cresswell JE. The influence of nectar and pollen availability on pollen transfer by individual flowers of oil seed rape (Brassica napus) when pollinated by bumblebees (Bombus lapidarius) Journal of Ecology. 1999;87(4):670–677. doi: 10.1046/j.1365-2745.1999.00385.x. DOI

Descamps C, Quinet M, Baijot A, Jacquemart AL. Temperature and water stress affect plant–pollinator interactions in Borago officinalis (Boraginaceae) Ecology and Evolution. 2018;8:3443–3456. doi: 10.1002/ece3.3914. PubMed DOI PMC

DuVal AS. Master’s thesis. 2015. Applied nitrogen effects on yellow mustard (Sinapis alba L.) production in the Willamette Valley.

Elliott SE, Irwin RE. Effects of flowering plant density on pollinator visitation, pollen receipt, and seed production in Delphinium barbeyi (Ranunculaceae) American Journal of Botany. 2009;96:912–919. doi: 10.3732/ajb.0800260. PubMed DOI

Fan HL, Sun WC, Yan N, Zhu HX, Wu JY, Zhang YH, Zeng J, Ye J, Liu YL. Analysis of self-compatibility in Sinapis alba (L.) Boiss. Proceedings of the 12th international rapeseed congress, Wuhan, China, 26–30; 2007. pp. 368–369.

Farré-Armengol G, Fernández-Martínez M, Filella I, Junker RR, Peñuelas J. Deciphering the biotic and climatic factors that influence floral scents: a systematic review of floral volatile emissions. Frontiers in Plant Science. 2020;11:1154. doi: 10.3389/fpls.2020.01154. PubMed DOI PMC

Fitter AH, Fitter RSR. Rapid changes in flowering time in British plants. Science. 2002;296:1689–1691. doi: 10.1126/science.1071617. PubMed DOI

Flacher F, Raynaud X, Hansart A, Geslin B, Motard B, Verstraet S, Bataille M, Dajoz I. Below-ground competition alters attractiveness of an insect-pollinated plant to pollinators. AoB Plants. 2020;12(4):plaa022. doi: 10.1093/aobpla/plaa022. PubMed DOI PMC

Fowler D, et al. The global nitrogen cycle in the twenty-first century. Philosophical Transactions of the Royal Society B. 2013;368:20130164. doi: 10.1098/rstb.2013.0164. PubMed DOI PMC

Galen C. High and dry: drought stress, sex-allocation trade-offs, and selection on flower size in the alpine wildflower Polemonium viscosum (Polemoniaceae) American Naturalist. 2000;156:72–83. doi: 10.1086/303373. PubMed DOI

Galloway JN, et al. Nitrogen cycles: past, present, and future. Biogeochemistry. 2004;70:153–226. doi: 10.1007/s10533-004-0370-0. DOI

Gardener MC, Gillman MP. The effects of soil fertilizer on amino acids in the floral nectar of corncockle, Agrostemma githago (Caryophyllaceae) Oikos. 2001;92:101–106. doi: 10.1034/j.1600-0706.2001.920112.x. DOI

Gardener MC, Gillman MP. The taste of nectar-a neglected area of pollination ecology. Oikos. 2002;98:552–557. doi: 10.1034/j.1600-0706.2002.980322.x. DOI

Gérard M, Vanderplanck M, Wood T, Michez D. Global warming and plant–pollinator mismatches. Emerging Topics in Life Sciences. 2020;4(1):77–86. doi: 10.1042/ETLS20190139. PubMed DOI PMC

Gómez JM, Perfectti F, Armas C, Narbona E, González-Megía SG, Navarro L, De Soto L, Torices R. Within-individual phenotypic plasticity in flowers fosters pollination niche shift. Nature Communications. 2020;11:4019. doi: 10.1038/s41467-020-17875-1. PubMed DOI PMC

Gray SB, Brady SM. Plant developmental responses to climate change. Arid Soil Research and Rehabilitation. 2016;2:49–58. PubMed

Grindeland JM, Sletvold N, Ims RA. Effects of floral display size and plant density on pollinator visitation rate in a natural population of Digitalis purpurea. Functional Ecology. 2005;19:383–390. doi: 10.1111/j.1365-2435.2005.00988.x. DOI

Güsewell S, Furrer R, Gehrig R, Pietragalla B. Changes in temperature sensitivity of spring phenology with recent climate warming in Switzerland are related to shifts of the preseason. Global Change Biology. 2017;23:5189–5202. doi: 10.1111/gcb.13781. PubMed DOI

Hatfield JL, Prueger JH. Temperature extremes: effect on plant growth and development. Weather and Climate Extremes. 2015;10(A):4–10. doi: 10.1016/j.wace.2015.08.001. DOI

Hedhly A. Sensitivity of flowering plant gametophytes to temperature fluctuations. Environmental and Experimental Botany. 2011;74:9–16. doi: 10.1016/j.envexpbot.2011.03.016. DOI

Hegland SJ, Nielsen A, Lázaro A, Bjerknes AL, Totland Ø. How does climate warming affect plant–pollinator interactions? Ecology Letters. 2009;12(2):184–195. doi: 10.1111/j.1461-0248.2008.01269.x. PubMed DOI

Hegland SJ, Totland Ø. Relationships between species’ floral traits and pollinator visitation in a temperate grassland. Oecologia. 2005;145:586–594. doi: 10.1007/s00442-005-0165-6. PubMed DOI

Hernández-Villa V, Vibrans H, Uscanga-Mortera E, Aguirre-Jaimes A. Floral visitors and pollinator dependence are related to floral display size and plant height in native weeds of central Mexico. Flora. 2020;262:151505. doi: 10.1016/j.flora.2019.151505. DOI

Holtsford TP, Ellstrand NC. Genetic and environmental variation in floral traits affecting outcrossing rate in Clarkia tembloriensis (Onagraceae) Evolution. 1992;46:216–225. doi: 10.1111/j.1558-5646.1992.tb01996.x. PubMed DOI

Hoover SER, Ladley JJ, Shchepetkina AA, Tisch M, Gieseg SP, Tylianakis JM. Warming, CO2, and nitrogen deposition interactively affect a plant–pollinator mutualism. Ecology Letters. 2012;15:227–234. doi: 10.1111/j.1461-0248.2011.01729.x. PubMed DOI

Inouye DW, Waller GD. Responses of honeybees (Apis mellifera) to amino acid solutions mimicking nectars. Ecology. 1984;65:618–625. doi: 10.2307/1941424. DOI

Jagadish SK, Bahuguna RN, Djanaguiraman M, Gamuyao R, Prasad PV, Craufurd PQ. Implications of high temperature and elevated CO2 on flowering time in plants. Frontiers in Plant Science. 2016;7:913. PubMed PMC

Jauzein P. Flore des champs cultivés. 2nd edition. Editions Quae; Versailles, France: 2011.

Junker RR, Blüthgen N, Brehm T, Binkenstein J, Paulus J, Schaefer MH, Stang M. Specialization on traits as basis for the niche-breadth of flower visitors and as structuring mechanism of ecological networks. Functional Ecology. 2013;27(2):329–341. doi: 10.1111/1365-2435.12005. DOI

Keasar T, Sadeh A, Shmida A. Variability in nectar production and standing crop, and their relation to pollinator visits in a Mediterranean shrub. Arthropod-Plant Interactions. 2008;2:117–123. doi: 10.1007/s11829-008-9040-9. DOI

Kehrberger S, Holzschuh A. Warmer temperatures advance flowering in a spring plant more strongly than emergence of two solitary spring bee species. PLOS ONE. 2019;14(6):e0218824. doi: 10.1371/journal.pone.0218824. PubMed DOI PMC

Klecka J, Hadrava J, Koloušková P. Vertical stratification of plant–pollinator interactions in a temperate grassland. PeerJ. 2018a;6:e4998. doi: 10.7717/peerj.4998. PubMed DOI PMC

Knight TM, Steets JA, Vamosi JC, Mazer SJ, Burd M, Campbell DR, Ashman TL, et al. Pollen limitation of plant reproduction: pattern and process. Annual Review of Ecology, Evolution and Systematics. 2005;36:467–497. doi: 10.1146/annurev.ecolsys.36.102403.115320. DOI

Lasky JR, Uriarte M, Muscarella R. Synchrony, compensatory dynamics, and the functional trait basis of phenological diversity in a tropical dry forest tree community: effects of rainfall seasonality. Environmental Research Letters. 2016;11:115003. doi: 10.1088/1748-9326/11/11/115003. DOI

Li Y, Guan K, Peng B, Franz TE, Wardlow B, Pan M. Quantifying irrigation cooling benefits to maize yield in the US Midwest. Global Change Biology. 2020;26:3065–3078. doi: 10.1111/gcb.15002. PubMed DOI

Lu NN, Li XH, Li L, Zhao ZG. Variation of nectar production in relation to plant characteristics in protandrous Aconitum gymnandrum. Journal of Plant Ecology. 2015;8(2):122–129. doi: 10.1093/jpe/rtv020. DOI

Mahan JR, McMicheal BL, Wanjura DF. Methods for reducing the adverse effects of temperature stress on plants: a review. Environmental and Experimental Botany. 1995;35:251–258. doi: 10.1016/0098-8472(95)00011-6. DOI

Majetic CJ, Fetters AM, Beck OM, Beck EF, Beam KM. Petuia floral trait plasticity in response to soil nitrogen content and subsequent impacts on insect visitation. Flora. 2017;232:183–193. doi: 10.1016/j.flora.2016.08.002. DOI

Meier U, Bleiholder H, Buhr L, Feller C, Hacks H, Hess M, Lancashire PD, Schnock U, Stauss R, Boom TVD. The BBCH system to coding the phenological growth stages of plants-history and publications. Journal fur Kulturpflanzen. 2009;2:41–52.

Mitchell RJ, Karron JD, Holmquist KG, Bell JM. The influence of Mimulus ringens floral display size on pollinator visitation patterns. Functional Ecology. 2004;18:116–124. doi: 10.1111/j.1365-2435.2004.00812.x. DOI

New B, Duthion C, Turc O. Phenological response of pea to water stress during reproductive development. Crop Science. 1994;34(1):141–146. doi: 10.2135/cropsci1994.0011183X003400010025x. DOI

NOAA National Centres for Environmental Information, State of the Climate: global Climate report for the Annual 2020, published online 2021, retrieved on September 13, 2021. https://www.ncdc.noaa.gov/sotc/global/202013 2021

Pacini E, Nepi M. Nectar production and presentation. In: Nicolson SW, Nepi M, Pacini E, editors. Nectaries and nectar. Springer; Dordrecht: 2007.

Parachnowitsch AL, Kessler A. Pollinators exert natural selection on flower size and floral display in Penstemon digitalis. New Phytologist. 2010;188(2):393–402. doi: 10.1111/j.1469-8137.2010.03410.x. PubMed DOI

Petanidou T, Van Laere A, Ellis WN, Smets E. What shapes amino acid and sugar composition in Mediterranean floral nectars? Oikos. 2006;115(1):155–169. doi: 10.1111/j.2006.0030-1299.14487.x. DOI

Pyke GH. Optimal foraging theory: a critical review. Annual Review of Ecology and Systematics. 1984;15(1):523–575. doi: 10.1146/annurev.es.15.110184.002515. DOI

Quemada M, Gabriel JL. Approaches for increasing nitrogen and water use efficiency simultaneously. Global Food Security. 2016;9:29–35. doi: 10.1016/j.gfs.2016.05.004. DOI

R Core Team . R Foundation for Statistical Computing; Vienna, Austria: 2020. R: a language and environment for statistical computing.

Rering CC, Franco JG, Yeater KM, Mallinger RE. Drought stress alters floral volatiles and reduces floral rewards, pollinator activity, and seed set in a global plant. Ecosphere. 2020;11(9):e03254

Reverté S, Retana J, Gómez JM, Bosch J. Pollinators show flower colour preferences but flowers with similar colours do not attract similar pollinators. Annals of Botany. 2016;118(2):249–257. doi: 10.1093/aob/mcw103. PubMed DOI PMC

Rusman Q, Poelman EH, Nowrin F, Polder G, Lucas-Barbosa D. Floral plasticity: herbivore-species-specific-induced changes in flower traits with contrasting effects on pollinator visitation. Plant, Cell and Environment. 2019;42(6):1882–1896. doi: 10.1111/pce.13520. PubMed DOI PMC

Rustad LE. The response of terrestrial ecosystems to global climate change: towards an integrated approach. Science of the Total Environment. 2008;404:222–235. doi: 10.1016/j.scitotenv.2008.04.050. PubMed DOI

Saavedra F, Inouye DW, Price MV, Harte J. Changes in flowering and abundance of Delphinium nuttallianum (Ranunculaceae) in response to a subalpine climate warming experiment. Global Change Biology. 2003;9:885–894. doi: 10.1046/j.1365-2486.2003.00635.x. DOI

Scaven VL, Rafferty NE. Physiological effects of climate warming on flowering plants and insect pollinators and potential consequences for their interactions. Current Zoology. 2013;59(3):418–426. doi: 10.1093/czoolo/59.3.418. PubMed DOI PMC

Schweiger O, Biesmeijer JC, Bommarco R, Hickler T, Hulme PE. Multiple stressors on biotic interactions: how climate change and alien species interact to affect pollination. Biological Reviews. 2010;85:777–795. PubMed

Scott-Wendt J, Chase RG, Hossner LR. Soil chemical variability in sandy Ustalfs in semi-arid Niger, West Africa. Soil Science. 1988;145(6):414–419.

Slamova I, Klecka J, Konvicka M. Diurnal behavior and habitat preferences of Erebia aethiops, an aberrant lowland species of a mountain butterfly clade. Journal of Insect Behavior. 2011;24(3):230–246. doi: 10.1007/s10905-010-9250-8. DOI

Snider JL, Oosterhuis DM. How does timing, duration, and severity of heat stress influence pollen-pistil interactions in angiosperms? Plant Signaling & Behavior. 2011;6(7):930–933. doi: 10.4161/psb.6.7.15315. PubMed DOI PMC

Takkis K, Tscheulin T, Tsalkatis P, Petanidou T. Climate change reduces nectar secretion in two common Mediterranean plants. AoB Plants. 2015;7:111. doi: 10.1093/aobpla/plv111. PubMed DOI PMC

Vasseur DA, De Long JP, Gilbert B, Greig HS, Harley CDG, McCann KS, Savage V, Tunney TD, O’Connor MI. Increased temperature variation poses a greater risk to species than climate warming. Proceedings of the Royal Society B: Biological Sciences. 2014;281(1779):2013–2612. PubMed PMC

Villarreal AG, Freeman CE. Effects of temperature and water stress on some floral nectar characteristics in Ipomopsis longiflora (Polemoniaceae) under controlled conditions. Botanical Gazatte. 1990;151:5–9. doi: 10.1086/337797. DOI

Wyatt R, Broyles SD, Derda GS. Environmental influences on nectar production in milkweeds (Asclepias syriaca and A. exaltata) American Journal of Botany. 1992;79:636–642. doi: 10.1002/j.1537-2197.1992.tb14605.x. DOI

Zimmermann M, Pyke GH. Reproduction in Polemonium: assessing the factors limiting seed set. American Naturalist. 1988;131:723–738. doi: 10.1086/284815. DOI

Pollen thermotolerance of a widespread plant, Lotus corniculatus, in response to climate warming: possible local adaptation of populations from different elevations

Zobrazit více v PubMed

figshare
10.6084/m9.figshare.13317686