Abstract
Many plant species respond to climate change by phenological shifts, usually with an earlier flowering onset. However, the variability in flowering responses to changed climatic conditions is large, and rare plant species, which are likely to have a low environmental tolerance, may be less able to shift their phenology than common ones. If plant species respond to climate change by shifting their flowering phenology, plant–pollinator interactions may become disrupted. However, it is vital for the reproduction of animal-pollinated plants, and thus for long-term population survival, that plants can attract pollinators. This might be especially difficult for rare species as they may depend on one or few pollinator species. To assess how climatic conditions affect the phenology of common and rare plant species, and whether the plant species attract potential pollinators, we assessed flowering onset and flower visitation in the lowland Botanical Garden of Bern, Switzerland, for 185 native plant species originating from different altitudinal zones. Plants from high elevations flowered earlier and showed more pronounced phenological shifts than plants from lower elevations, independent of species rarity. The probability, number, and duration of flower visits and the number of flower-visitor groups were independent of the altitudinal zone of plant origin and of species rarity. The composition of flower-visitor groups did also not depend on the altitudinal zone of plant origin and on species rarity. Thus, rare and common alpine plants may generally respond to climate change by an earlier flowering onset, and may be able to establish novel interactions with pollinators.
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References
Alarcón R, Waser NM, Ollerton J (2008) Year-to-year variation in the topology of a plant–pollinator interaction network. Oikos 117:1796–1807
Ames GM, Wall WA, Hohmann MG, Wright JP (2016) Trait space of rare plants in a fire-dependent ecosystem. Conserv Biol 31:903–911. https://doi.org/10.1111/cobi.12867
Anderson JT, Inouye DW, McKinney AM, Colautti RI, Mitchell-Olds T (2012) Phenotypic plasticity and adaptive evolution contribute to advancing flowering phenology in response to climate change. Proc R Soc Lond Ser B Biol Sci 279:3843–3852
Bascompte J, Jordano P, Olesen JM (2006) Asymmetric coevolutionary networks facilitate biodiversity maintenance. Science 312:431–433
Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48
Baythavong BS, Stanton ML (2010) Characterizing selection on phenotypic plasticity in response to natural environmental heterogeneity. Evolution 64:2904–2920
Blüthgen N, Menzel F, Hovestadt T, Fiala B, Blüthgen N (2007) Specialization, constraints, and conflicting interests in mutualistic networks. Curr Biol 17:341–346. https://doi.org/10.1016/j.cub.2006.12.039
Burgess K, Etterson J, Galloway L (2007) Artificial selection shifts flowering phenology and other correlated traits in an autotetraploid herb. Heredity 99:641–648
Burkle LA, Marlin JC, Knight TM (2013) Plant-pollinator interactions over 120 years: loss of species, co-occurrence and function. Science 339:1611–1615
CaraDonna PJ, Iler AM, Inouye DW (2014) Shifts in flowering phenology reshape a subalpine plant community. Proc Natl Acad Sci 111:4916–4921
Chevin L-M, Hoffmann AA (2017) Evolution of phenotypic plasticity in extreme environments. Philos Trans R Soc B Biol Sci 372. https://doi.org/10.1098/rstb.2016.0138
Cleland EE et al (2012) Phenological tracking enables positive species responses to climate change. Ecology 93:1765–1771
Delnevo N, Petraglia A, Carbognani M, Vandvik V, Halbritter AH (2017) Plastic and genetic responses to shifts in snowmelt time affects the reproductive phenology and growth of Ranunculus acris Perspect Plant Ecol Evol Syst. https://doi.org/10.1016/j.ppees.2017.07.005
Dicks L, Corbet S, Pywell R (2002) Compartmentalization in plant–insect flower visitor webs. J Anim Ecol 71:32–43
Diez JM et al (2012) Forecasting phenology: from species variability to community patterns. Ecol Lett 15:545–553
Dunne JA, Harte J, Taylor KJ (2003) Subalpine meadow flowering phenology responses to climate change: integrating experimental and gradient methods. Ecol Monogr 73:69–86
Dupont YL, Padrón B, Olesen JM, Petanidou T (2009) Spatio-temporal variation in the structure of pollination networks. Oikos 118:1261–1269
Enßlin A, Sandner TM, Matthies D (2011) Consequences of ex situ cultivation of plants: genetic diversity, fitness and adaptation of the monocarpic Cynoglossum officinale L in botanic gardens. Biol Conserv 144:272–278
Fitter A, Fitter R (2002) Rapid changes in flowering time in British plants. Science 296:1689–1691
Forrest J, Miller-Rushing AJ (2010) Toward a synthetic understanding of the role of phenology in ecology and evolution. Philos Trans R Soc Lond B Biol Sci 365:3101–3112
Ghazoul J (2006) Floral diversity and the facilitation of pollination. J Ecol 94:295–304
Giménez-Benavides L, García-Camacho R, Iriondo JM, Escudero A (2011) Selection on flowering time in Mediterranean high-mountain plants under global warming. Evol Ecol 25:777–794
Gugger S, Kesselring H, Stöcklin J, Hamann E (2015) Lower plasticity exhibited by high- versus mid-elevation species in their phenological responses to manipulated temperature and drought. Ann Bot 116:953–962. https://doi.org/10.1093/aob/mcv155
Hallmann CA et al (2017) More than 75 percent decline over 27 years in total flying insect biomass in protected areas. PLOS One 12:e0185809. https://doi.org/10.1371/journal.pone.0185809
Hegland SJ, Nielsen A, Lázaro A, Bjerknes AL, Totland Ø (2009) How does climate warming affect plant-pollinator interactions? Ecol Lett 12:184–195
Hülber K, Winkler M, Grabherr G (2010) Intraseasonal climate and habitat-specific variability controls the flowering phenology of high alpine plant species. Funct Ecol 24:245–252
Inouye DW (2008) Effects of climate change on phenology, frost damage, and floral abundance of montane wildflowers. Ecology 89:353–362
IPCC (2007) Intergovernmental Panel On Climate Change, Fourth Assessment Report, Climate Change 2007: Syntheses Report. UNEP, Geneva
Kaiser-Bunbury CN, Muff S, Memmott J, Müller CB, Caflisch A (2010) The robustness of pollination networks to the loss of species and interactions: a quantitative approach incorporating pollinator behaviour. Ecol Lett 13:442–452
Kudo G, Ida TY (2013) Early onset of spring increases the phenological mismatch between plants and pollinators. Ecology 94:2311–2320
Landolt E (2003) Unsere Alpenflora vol 7. SAC-Verlag Schweizer Alpen-Club, Bern
Landolt E et al (2010) Flora indicativa–ecological indicator values and biological attributes of the flora of Switzerland and the Alps. Haupt, Bern
Lauterbach D, Burkart M, Gemeinholzer B (2012) Rapid genetic differentiation between ex situ and their in situ source populations: an example of the endangered Silene otites (Caryophyllaceae. Bot J Linn Soc 168:64–75
Lázaro-Nogal A, Matesanz S, Godoy A, Pérez-Trautman F, Gianoli E, Valladares F (2015) Environmental heterogeneity leads to higher plasticity in dry-edge populations of a semi-arid Chilean shrub: insights into climate change responses. J Ecol 103:338–350
Lunn DJ, Thomas A, Best N, Spiegelhalter D (2000) WinBUGS-a Bayesian modelling framework: concepts, structure, and extensibility. Stat Comput 10:325–337
Matesanz S, Valladares F (2014) Ecological and evolutionary responses of Mediterranean plants to global change. Environ Exp Bot 103:53–67
Memmott J, Waser NM (2002) Integration of alien plants into a native flower-pollinator visitation web. Proc R Soc Lond Ser B Biol Sci 269:2395–2399. https://doi.org/10.1098/rspb.2002.2174
Memmott J, Craze PG, Waser NM, Price MV (2007) Global warming and the disruption of plant–pollinator interactions. Ecol Lett 10:710–717
Mitchell RJ, Flanagan RJ, Brown BJ, Waser NM, Karron JD (2009) New frontiers in competition for pollination. Ann Bot 103:1403–1413
Moser D, Gygax A, Bäumler B, Wyler N, Palese R (2002) Red List of threatened ferns and flowering plants in Switzerland Bundesamt für Umwelt, Wald und Landschaft, Bern, Zentrum des Datenverbundnetzes der Schweizer Flora. Chambésy, Conservatoire et Jardin Botaniques de la Ville de Genève, Chambésy
Ntzoufras I (2011) Bayesian modeling using WinBUGS, vol 698. Wiley, New Jersey
Ollerton J (2017) Pollinator diversity: distribution, ecological function, and conservation. Ann Rev Ecol Evol Syst 48:353–376. https://doi.org/10.1146/annurev-ecolsys-110316-022919
Orians GH (1997) Evolved consequences of rarity. The biology of rarity. Springer, Berlin, pp 190–208
Parmesan C (2006) Ecological and evolutionary responses to recent climate change. Annu Rev Ecol Evol Syst 37:637–669
Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature 421:37–42
Pau S et al (2011) Predicting phenology by integrating ecology, evolution and climate science. Global Change Biol 17:3633–3643
Petanidou T, Kallimanis AS, Tzanopoulos J, Sgardelis SP, Pantis JD (2008) Long-term observation of a pollination network: fluctuation in species and interactions, relative invariance of network structure and implications for estimates of specialization. Ecol Lett 11:564–575
Petanidou T, Kallimanis AS, Sgardelis SP, Mazaris AD, Pantis JD, Waser NM (2014) Variable flowering phenology and pollinator use in a community suggest future phenological mismatch. Acta Oecol 59:104–111
Phillips RD, Peakall R, Hutchinson MF, Linde CC, Xu T, Dixon KW, Hopper SD (2014) Specialized ecological interactions and plant species rarity: the role of pollinators and mycorrhizal fungi across multiple spatial scales. Biol Conserv 169:285–295
R Core Team (2012) A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Razanajatovo M, Föhr C, Fischer M, Prati D, van Kleunen M (2015) Non-naturalized alien plants receive fewer flower visits than naturalized and native plants in a Swiss botanical garden. Biol Conserv 182:109–116
Rixen C, Dawes MA, Wipf S, Hagedorn F (2012) Evidence of enhanced freezing damage in treeline plants during six years of CO2 enrichment and soil warming. Oikos 121:1532–1543
Sargent RD, Otto SP (2006) The role of local species abundance in the evolution of pollinator attraction in flowering plants. Am Nat 167:67–80
Scheepens J, Stöcklin J (2013) Flowering phenology and reproductive fitness along a mountain slope: maladaptive responses to transplantation to a warmer climate in Campanula thyrsoides. Oecologia 171:679–691
Schielzeth H (2010) Simple means to improve the interpretability of regression coefficients. Methods Ecol Evol 1:103–113
Schmid SF, Stöcklin J, Hamann E, Kesselring H (2017) High-elevation plants have reduced plasticity in flowering time in response to warming compared to low-elevation congeners. Basic Appl Ecol 21:1–12. https://doi.org/10.1016/j.baae.2017.05.003
Sedlacek J et al (2015) The response of the alpine dwarf shrub Salix herbacea to altered snowmelt timing: lessons from a multi-site transplant experiment. PLOS One 10:e0122395
Sheth SN, Angert AL (2014) The evolution of environmental tolerance and range size: a comparison of geographically restricted and widespread Mimulus. Evol 68:2917–2931. https://doi.org/10.1111/evo.12494
Springate DA, Kover PX (2014) Plant responses to elevated temperatures: a field study on phenological sensitivity and fitness responses to simulated climate warming. Global Change Biol 20:456–465
Sultan SE (2001) Phenotypic plasticity for fitness components in Polygonum species of contrasting ecological breadth. Ecology 82:328–343. https://doi.org/10.1890/0012-9658(2001)082[0328:PPFFCI]2.0.CO;2
van Kleunen M, Dawson W, Bossdorf O, Fischer M (2014) The more the merrier: multi-species experiments in ecology Basic. Appl Ecol 15:1–9
Venables W, Ripley B (2002) Modern applied statistics with S. Fourth Edition. Springer, New York
Vilà M, Bartomeus I, Dietzsch AC, Petanidou T, Steffan-Dewenter I, Stout JC, Tscheulin T (2009) Invasive plant integration into native plant–pollinator networks across Europe. Proc R Soc Lond Ser B Biol Sci 276:3887–3893
Wolkovich EM, Cook BI, Davies TJ (2014) Progress towards an interdisciplinary science of plant phenology: building predictions across space time species diversity. New Phytol 201:1156–1162
Zuur A, Ieno E, Walker N, Saveliev A, Smith G (2009) Mixed effects models and extensions in ecology with R. Springer, New York
Acknowledgements
We thank all volunteers who helped with the data collection; the Botanical Garden of Bern for allowing the flower-visitor observations; Corina del Fabbro for statistical advice; Andreas Ensslin and Steffen Boch for helpful comments on the manuscript. M. R. thanks the German Research Foundation DFG for funding (RA 3009/1–1).
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Razanajatovo, M., Föhr, C., van Kleunen, M. et al. Phenological shifts and flower visitation of 185 lowland and alpine species in a lowland botanical garden. Alp Botany 128, 23–33 (2018). https://doi.org/10.1007/s00035-018-0201-x
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DOI: https://doi.org/10.1007/s00035-018-0201-x