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Ranunculus glacialis L.: successful reproduction at the altitudinal limits of higher plant life

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Abstract

Biodiversity decreases with increasing altitude, mainly because of the increasingly adverse climate. In the European Alps, only a few plant species occur above 4,000 m a.s.l., among these is Ranunculus glacialis L. Current studies have shown that R. glacialis has a highly conservative growth strategy and low developmental plasticity in response to different dates of snowmelt. Therefore, it was of particular interest to observe whether this strategy is maintained at higher altitudes and to reveal the reproductive limits. We examined the effect of the date of snowmelt on reproductive development and reproductive success in R. glacialis over several years at two subnival sites (2,650 and 2,880 m a.s.l.) and at a nival site (3,440 m a.s.l.) in the Austrian Alps. At the subnival sites, reproductive performance was relatively stable (prefloration period, i.e. snowmelt to onset of anthesis, 2–3 weeks; postfloration period, i.e. onset of anthesis until fruit maturity, 4–5 weeks). Depending on the date of flowering, the mean seed/ovule (S/O) ratio was 0.5–0.8. The temporal safety margin between seed maturation and the onset of winter conditions was at least 1 month. The situation was quite different in the nival zone: the prefloration period usually lasted 1 month, anthesis up to 2 weeks, and seed development 6–7 weeks; when seeds matured in time, the S/O ratio was 0.4–0.6. Overall, R. glacialis shows a high developmental plasticity. At higher altitudes, R. glacialis can double the time taken for seed development but runs a high risk of seeds not maturing in time.

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Abbreviations

S/O ratio:

Seed/ovule ratio

DAA:

Days after onset of anthesis

SN-L:

Subnival low

SN-H:

Subnival high

doy:

Day of year

References

  • Anchisi E (1985) Quatrieme contribution à l´étude de la flore valaisanne. Bull Murithienne 102:115–126

    Google Scholar 

  • Arroyo MTK, Armesto J, Primack R (1985) Community studies in pollination ecology in the high temperate Andes of Central Chile. II. Effect of temperature on visitation rates and pollination possibilities. Plant Syst Evol 149:187–203

    Article  Google Scholar 

  • Baskin CC, Baskin JM (1998) Seeds: ecology, biogeography, and evolution of dormancy and germination. Academic, San Diego, California, pp 1–666

    Google Scholar 

  • Billings WD, Bliss LC (1959) An alpine snowbank environment and its effects on vegetation, plant development, and productivity. Ecology 40:388–397

    Article  Google Scholar 

  • Boesewinkel FD, Bouman F (1995) The seed: structure and function. In: Kigel J, Galili G (eds) Seed development and germination. Marcel Dekker Inc., New York, pp 1–24

    Google Scholar 

  • Cleve A (1901) Zum Pflanzenleben in nordschwedischen Hochgebirgen. Bihang till Kungliga Svenska Vetenskapsakademien Handlingar, Vol. 26/III. Norstedt, Stockholm, pp. 1–105

  • Cooper EJ (2004) Out of sight, out of mind: thermal acclimation of root respiration in arctic Ranunculus. Arct Antarct Alp Res 36:308–313

    Article  Google Scholar 

  • Cosendai A.-C., Hörandl E (2010) Cytotype stability, facultative apomixix and geographical parthenogenesis in Ranunculus kuepferi (Ranunculaceae). doi:10.1093/aob/mcp304

  • Crawford RMM (2008) Plants at the Margin. Cambridge University Press, Cambridge, pp 1–478

    Google Scholar 

  • Crawford RMM, Smith LC (1997) Responses of some high Arctic shore plants to variable lengths of growing season. Opera Bot 132:201–214

    Google Scholar 

  • Crawford RMM, Chapman HM, Abbott RJ, Balfour J (1993) Potential impact of climatic warming on Arctic vegetation. Flora 188:367–381

    Google Scholar 

  • Danks HV (2004) Seasonal adaptations in Arctic insects. Integr Comp Biol 44:85–94

    Article  Google Scholar 

  • Diemer M (1992) Population dynamics and spatial arrangement of Ranunculus glacialis L., an alpine perennial herb, in permanent plots. Vegetatio 103:159–166

    Google Scholar 

  • Engell K (1995) Embryo morphology of the Ranunculaceae. Plant Syst Evol (Suppl) 9:207–216

    Google Scholar 

  • Escaravage N, Wagner J (2004) Pollination effectiveness and pollen dispersal in a Rhododendron ferrugineum (Ericaceae) population. Plant Biol 6:606–615

    Article  CAS  PubMed  Google Scholar 

  • Forbis TA, Diggle PK (2001) Subnivean embryo development in the alpine herb Caltha leptosepala (Ranunculaceae). Can J Bot 79:635–642

    Article  Google Scholar 

  • Förster P (1997) Die Keimpflanzen der Tribus Ranunculaceae DC. und der Tribus Adonideae Kunth (Ranunculaceae). Flora 192:133–142

    Google Scholar 

  • Galen C, Stanton M (1991) Consequences of emergence phenology for reproductive success in Ranunculus adoneus (Ranunculaceae). Am J Bot 78:978–988

    Article  Google Scholar 

  • Galen C, Stanton M (1995) Responses of snowbed plant species to changes in growing-season length. Ecology 76:1546–1557

    Article  Google Scholar 

  • García-Camacho R, Totland Ø (2009) Pollen limitation in the alpine: a meta-analysis. Arct Antarct Alp Res 41:103–111

    Article  Google Scholar 

  • Grabherr G, Gottfried M, Gruber A, Pauli H (1995) Patterns and current changes in alpine plant diversity. In: Chapin FS III, Körner C (eds) Arctic and alpine biodiversity. Ecological studies 113. Springer, Berlin, pp 167–181

    Google Scholar 

  • Heer O (1885) Über die nivale Flora der Schweiz. Neue Denkschr. Allg. Schweiz. Ges. Gesamt Naturwiss 24:4–114

    Google Scholar 

  • Herr JM (1971) A new clearing-squash technique for the study of ovule development in angiosperms. Am J Bot 58:785–790

    Article  Google Scholar 

  • Hörandl E (2008) Evolutionary implications of self-compatibility and reproductive fitness in the apomictic Ranunculus auricomus polyploid complex (Ranunculaceae). Int J Plant Sci 169:1219–1228

    Article  PubMed  Google Scholar 

  • Hörandl E, Paun O (2007) Patterns and sources of genetic diversity in apomictic plants: implications for evolutionary potentials. In: Hörandl E, Grossniklaus U, van Dijk PJ, Sharbel TF (eds) Apomixis: evolution, mechanisms and perspectives. Monographs in Plant Systematics, Regnum Vegetabile volume 147. ARG Gantner Verlag, Rugell, Rugell, pp 169–194

    Google Scholar 

  • Hörandl E, Paun O, Johansson JT, Lehnebach C, Armstrong T, Chen L, Lockhart P (2005) Phylogenetic relationships and evolutionary traits in Ranunculus s.l. (Ranunculaceae) inferred from ITS sequence analysis. Molec Phylog Evol 36:305–327

    Article  CAS  Google Scholar 

  • Huelber K, Gottfried M, Pauli H, Reiter K, Winkler M, Grabherr G (2006) Phenological responses of snowbed species to snow removal dates in the Central Alps: implications for climate warming. Arct Antarct Alp Res 38:99–103

    Article  Google Scholar 

  • Inouye D, Wielgolaski FE (2003) High altitude climates. In: Schwartz MD (ed) Phenology: an integrative environmental science. Kluwer Academic Publishers, Dordrecht, pp 195–214

    Google Scholar 

  • Inouye D, Morales MA, Dodge GJ (2002) Variation in timing and abundance of flowering by Delphinium barbeyi Huth (Ranunculaceae): the roles of snowpack, frost, and La Niña, in the context of climate change. Oecologia 130:543–550

    Article  Google Scholar 

  • Itagaki T, Sakai S (2006) Relationship between floral longevity and sex allocation among flowers within inflorescences in Aquilegia buergeriana var. oxysepala (Ranunculaceae). Am J Bot 93:1320–1327

    Article  Google Scholar 

  • Järvinen A (1989) The life history of Ranunculus glacialis, an arctic–alpine perennial herb, in Finnish Lapland. Holarct Ecol 12:152–162

    Google Scholar 

  • Johri BM, Ambegaokar KB, Srivastava PS (1992) Comparative embryology of angiosperms, vol 1. Springer, Berlin, pp 1–614

    Google Scholar 

  • Körner C (2003) Alpine plant life, 2nd edn. Springer, Berlin, pp 1–349

    Google Scholar 

  • Kudo G (1991) Effects of snow-free period on the phenology of alpine plants inhabiting snow patches. Arct Alp Res 23:436–443

    Article  Google Scholar 

  • Kudo G, Suzuki S (1999) Flowering phenology of alpine plant communities along a gradient of snowmelt timing. Polar Biosci 12:100–113

    Google Scholar 

  • Ladinig U, Wagner J (2005) Sexual reproduction of the high mountain plant Saxifraga moschata Wulfen at varying lengths of the growing season. Flora 200:502–515

    Google Scholar 

  • Ladinig U, Wagner J (2007) Timing of sexual reproduction and reproductive success in the high-mountain plant Saxifraga bryoides L. Plant Biol 9:683–693

    Article  CAS  PubMed  Google Scholar 

  • Landolt E (1992) Unsere Alpenflora. Fischer Verlag, Stuttgart, Jena, pp 1–318

    Google Scholar 

  • Larcher W, Wagner J (1976) Temperaturgrenzen der CO2-Aufnahme und Temperaturresistenz der Blätter von Gebirgspflanzen im vegetationsaktiven Zustand. Oecol Plant 11:361–374

    Google Scholar 

  • Larcher W, Wagner J (2009) High mountain bioclimate: temperatures near the ground recorded from the timberline to the nival zone in the Central Alps. Contrib Nat Hist Berne 12:857–874

    Google Scholar 

  • Larcher W, Wagner J, Lütz C (1997) Effect of heat on photosynthesis, dark respiration and cellular ultrastructure of the arctic-alpine psychrophyte Ranunculus glacialis. Photosynthetica 34:219–232

    Article  CAS  Google Scholar 

  • Larcher W, Kainmüller C, Wagner J (2010) Survival types of high mountain plants under extreme temperatures. Flora 205:3–18

    Google Scholar 

  • McCall C, Primack RB (1992) Influence of flower characteristics, weather, time of day, and season on insect visitation rates in three plant communities. Am J Bot 79:434–442

    Article  Google Scholar 

  • McGraw JB, Antonovics J (1983) Experimental ecology of Dryas octopetala ecotypes. I. Ecotypic differentiation and life-cycle stages of selection. J Ecol 71:879–897

    Article  Google Scholar 

  • Meusel H, Jäger E, Weinert E (1965) Vergleichende Chorologie der Zentraleuropäischen Flora. Karten. Gustav Fischer Verlag, Jena, pp 1–258

    Google Scholar 

  • Molau U (1993) Relationships between flowering phenology and life history strategies in tundra plants. Arct Alp Res 25:391–402

    Article  Google Scholar 

  • Molau U (1997) Phenology and reproductive success in arctic plants: susceptibility to climate change. In: Oechel WC, Callaghan T, Gilmanov T, Holten JI, Maxwell B, Molau U, Sveinbjörnsson B (eds) Global change and arctic terrestrial ecosystems. Ecological studies 124. Springer, Berlin, pp 153–170

    Google Scholar 

  • Moser W, Brzoska W, Zachhuber K, Larcher W (1977) Ergebnisse des IBP-Projekts Hoher Nebelkogel 3184 m. Sitzungsber Österr Akad Wiss, Math-naturwiss Klasse Abt I 186:387–419

    Google Scholar 

  • Muñoz A, Arroyo MTK (2006) Pollen limitation and spatial variation of reproductive success in the insect-pollinated shrub Chuquiraga oppositifolia (Asteraceae) in the Chilean Andes. Arct Antarct Alp Res 38:608–613

    Article  Google Scholar 

  • Ozenda P (1988) Die Vegetation der Alpen. Elsevier, München, pp 1–353

    Google Scholar 

  • Pauli H, Gottfried M, Grabherr G (1999) Vascular plant distribution patterns at the low-temperature limits of plant life—the alpine–nival ecotone of Mount Schrankogel (Tyrol, Austria). Phytocoenologia 29:297–325

    Google Scholar 

  • Paun O, Lehnebach C, Johansson JT, Lockhart P, Hörandl E (2005) Phylogenetic relationships and biogeography of Ranunculus and allied genera (Ranunculaceae) in the Mediterranean region and in the European Alpine System. Taxon 54:911–930

    Article  Google Scholar 

  • Philipp M, Böcher J, Mattsson O, Woodell SR (1990) A quantitative approach to the sexual reproductive biology and population structure in some arctic flowering plants: Dryas integrifolia, Silene acaulis and Ranunculus nivalis. Medd Grønland, Biosci 34:3–60

    Google Scholar 

  • Pickering CM (1997a) Breeding systems of Australian Ranunculus in the alpine region. Nord J Bot 17:613–620

    Article  Google Scholar 

  • Pickering CM (1997b) Reproductive strategies and constraints of alpine plants as illustrated by five species of Australian alpine Ranunculus. Opera Bot 132:101–108

    Google Scholar 

  • Pluess AR, Schütz W, Stöcklin J (2005) Seed weight increases with altitude in the Swiss Alps between related species but not among populations of individual species. Oecologia 144:55–61

    Article  PubMed  Google Scholar 

  • Prock S, Körner C (1996) A cross-continental comparison of phenology, leaf dynamics and dry matter allocation in arctic and temperate zone herbaceous plants from contrasting altitudes. Ecol Bull 45:93–103

    CAS  Google Scholar 

  • Richards AJ (1997) Plant breeding systems. Chapman & Hall, London, pp 1–529

    Google Scholar 

  • Robertson AW, Lloyd DG (1993) Rates of pollen deposition and removal in Myosotis colensoi. Funct Ecol 7:549–559

    Article  Google Scholar 

  • Rønning OI (1996) The flora of Svalbard. Norwegian Polar Institute, Oslo, pp 1–184

    Google Scholar 

  • Schönswetter P, Tribsch A, Stehlik I, Niklfeld H (2004) Glacial history of high alpine Ranunculus glacialis (Ranunculaceae) in the European Alps in a comparative phylogeographical context. Biol J Linn Soc 81:183–195

    Article  Google Scholar 

  • Stanton ML, Galen C (1997) Life on the edge: adaptation versus environmentally mediated gene flow in the snow buttercup, Ranunculus adoneus. Am Nat 150:143–178

    Article  Google Scholar 

  • Steinacher G, Wagner J (2010) Flower longevity and duration of pistil receptivity in high mountain plants. doi:10.1016/j.flora.2009.12.012

  • Taschler D, Neuner G (2004) Summer frost resistance and freezing patterns measured in situ in leaves of major alpine plant growth forms in relation to their upper distribution boundary. Plant Cell Environ 27:737–746

    Article  Google Scholar 

  • Totland Ø (1993) Pollination in alpine Norway: flowering phenology, insect visitors, and visitation rates in two plant communities. Can J Bot 71:1072–1079

    Google Scholar 

  • Totland Ø (1994) Intraseasonal variation in pollination intensity and seed set in an alpine population of Ranunculus acris in southwestern Norway. Ecography 17:159–165

    Article  Google Scholar 

  • Totland Ø (2001) Environment-dependent pollen limitation and selection on floral traits in an alpine species. Ecology 82:2233–2244

    Article  Google Scholar 

  • Totland Ø, Alatalo JM (2002) Effects of temperature and date of snowmelt on growth, reproduction, and flowering phenology in the arctic/alpine herb, Ranunculus glacialis. Oecologia 133:168–175

    Article  Google Scholar 

  • Totland Ø, Schulte-Herbrüggen B (2003) Breeding system, insect flower visitation, and floral traits of two alpine Cerastium species in Norway. Arct Antarct Alp Res 35:242–247

    Article  Google Scholar 

  • Wagner J, Reichegger B (1997) Phenology and seed development of the alpine sedges Carex curvula and Carex firma in response to contrasting topoclimates. Arct Alp Res 29:291–299

    Article  Google Scholar 

  • Wiens D (1984) Ovule survivorship, brood size, life history, breeding systems, and reproductive success in plants. Oecologia 64:47–53

    Article  Google Scholar 

  • Yakovlev MS (1981) Comparative embryology of flowering plants. Vol 1, Winteraceae—Juglandaceae. Nauka, St Petersburg, pp. 1–263

  • Zimmermann W (1975) Ranunculaceae. In: Rechinger KH, Damboldt J (eds) Gustav Hegi—Illustrierte Flora von Mitteleuropa. Vol 3/3, Paul Parey, Berlin-Hamburg, pp 53–341

  • Zoller H, Lenzin H, Rusterholz H-P, Stöcklin J (2005) Increasing population density and seed production with altitude in Eritrichium nanum (Boraginaceae)—an arctic–alpine obligatory seeder. Arct Antarct Alp Res 37:41–48

    Article  Google Scholar 

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Acknowledgements

This study was funded by the Austrian Science Foundation (FWF) as part of the project “Diversity of sexual reproduction in high mountain plants” (P15595-B3). We thank Stefanie Erler, Daniela Hosp, and Stephanie Widmann for their help with fieldwork and for providing data. We thank E. Hörandl and M. Akhalkatsi for valuable suggestions on the manuscript. Thanks also to the Stubaier Gletscherbahn and the Zillertaler Gletscherbahn for free transportation by cable car.

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The authors declare that they have no conflict of interest.

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Correspondence to Johanna Wagner.

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This paper is dedicated to Professor Cornelius Lütz on the occasion of his 65th birthday.

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Wagner, J., Steinacher, G. & Ladinig, U. Ranunculus glacialis L.: successful reproduction at the altitudinal limits of higher plant life. Protoplasma 243, 117–128 (2010). https://doi.org/10.1007/s00709-009-0104-1

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