Pros and cons of using a standard protocol to test germination of alpine species

Alexander JM, Diez JM, Levine JM (2015) Novel competitors shape species’ responses to climate change. Nature 525:515–518. https://doi.org/10.1038/nature14952

Alexander JM, Chalmandrier L, Lenoir J, Burgess TI, Essl F, Haider S, Kueffer C, McDougall K, Milbau A, Nuñez MA, Pauchard A, Rabitsch W, Rew LJ, Sanders NJ, Pellissier L (2018) Lags in the response of mountain plant communities to climate change. Glob Chang Biol 24:563–579. https://doi.org/10.1111/gcb.13976

Alsos IG, Müller E, Eidesen PB (2013) Germinating seeds or bulbils in 87 of 113 tested arctic species indicate potential for ex situ seed bank storage. Polar Biol 36:819–830. https://doi.org/10.1007/s00300-013-1307-7

Amen RD (1966) The extent and role of seed dormancy in alpine plants. Q Rev Biol 41:271–281. https://doi.org/10.1086/405055

Andersson L, Milberg P (1998) Variation in seed dormancy among mother plants, populations and years of seed collection. Seed Sci Res 8:29–38. https://doi.org/10.1017/s0960258500003883

Auguie B, Antonov A (2017) Package gridExtra. https://cran.r-project.org/web/packages/gridExtra/gridExtra.pdf. Accessed 14 Nov 2019

Baskin JM, Baskin CC (2004) A classification system for seed dormancy. Seed Sci Res 14:1–16. https://doi.org/10.1079/ssr2003150

Baskin CC, Baskin JM (2005) Underdeveloped embryos in dwarf seeds and implications for assignment to dormancy class. Seed Sci Res 15:357–360. https://doi.org/10.1079/ssr2005224

Baskin CC, Baskin JM (2014) Seeds: ecology, biogeography, and evolution of dormancy and germination, 2nd edn. Elsevier, London

Bernareggi G, Carbognani M, Mondoni A, Petraglia A (2016) Seed dormancy and germination changes of snowbed species under climate warming: the role of pre-and post-dispersal temperatures. Ann Bot 118:529–539. https://doi.org/10.1093/aob/mcw125

Billings WD, Mooney HA (1968) The ecology of arctic and alpine plants. Biol Rev 43:481–529. https://doi.org/10.1111/j.1469-185X.1968.tb00968.x

Bliss LC (1958) Seed germination in arctic and alpine species. Arctic 11:180. https://doi.org/10.14430/arctic3743

Brusa G, Ceriani R, Cerabolini B (2007) Seed germination in a narrow endemic species (Telekia speciosissima, Asteraceae): implications for ex situ conservation. Plant Biosyst 141:56–61. https://doi.org/10.1080/11263500601153495

Bu H, Chen X, Xu X, Liu K, Jia P, Du G (2007) Seed mass and germination in an alpine meadow on the eastern Tsinghai-Tibet plateau. Plant Ecol 191:127–149. https://doi.org/10.1007/s11258-006-9221-5

Caccianiga M, Luzzaro A, Pierce S, Ceriani RM, Cerabolini B (2006) The functional basis of a primary succession resolved by CSR classification. Oikos 112:10–20. https://doi.org/10.1111/j.0030-1299.2006.14107.x

Casazza G, Giordani P, Benesperi R, Foggi B, Viciani D, Filigheddu R, Farris E, Bagella S, Pisanu S, Mariotti MG (2014) Climate change hastens the urgency of conservation for range-restricted plant species in the central-northern Mediterranean region. Biol Conserv 179:129–138. https://doi.org/10.1016/j.biocon.2014.09.015

Cavieres LA, Arroyo MTK (2000) Seed germination response to cold stratification period and thermal regime in Phacelia secunda (Hydrophyllaceae): altitudinal variation in the mediterranean andes of central Chile. Plant Ecol 149:1–8. https://doi.org/10.1023/A:1009802806674

Cavieres LA, Sierra-Almeida A (2018) Assessing the importance of cold-stratification for seed germination in alpine plant species of the High-Andes of central Chile. Perspect Plant Ecol Evol Syst 30:125–131. https://doi.org/10.1016/j.ppees.2017.09.005

Coomes DA, Grubb PJ (2003) Colonization, tolerance, competition and seed-size variation within functional groups. Trends Ecol Evol 18:283–291. https://doi.org/10.1016/S0169-5347(03)00072-7

Donohue K, Rubio de Casas R, Burghardt L, Kovach K, Willis CG (2010) Germination, postgermination adaptation, and species ecological ranges. Annu Rev Ecol Evol Syst 41:293–319. https://doi.org/10.1146/annurev-ecolsys-102209-144715

ENSCONET (2009a) ensconet seed collecting manual for wild species. https://www.publicgardens.org/resources/ensconet-seed-collecting-manual-wild-species. Accessed 4 Feb 2020

ENSCONET (2009b) ENSCONET Curation protocols & Recommendations. https://ensconet.maich.gr/PDF/Curation_protocol_English.pdf. Accessed 4 Feb 2020

Eriksson O (1999) Seed size variation and its effect on germination and seedling performance in the clonal herb Convallaria majalis. Acta Oecol 20:61–66. https://doi.org/10.1016/S1146-609X(99)80016-2

Erschbamer B, Pfattner M (2002) Das Keimverhalten von alpinen Arten in der Klimakammer und im Gelände Germination characteristics of alpine species in the growth chamber and in the field site. Ber Nat Med Verein Innsbruck 89:87–97

Erschbamer B, Caccianiga MS (2017) Glacier forelands: lessons of plant population and community development. In: Cánovas FM, Lüttge U, Matyssek R (eds) Progress in botany, vol 78. Springer, Cham, pp 259–284

Erschbamer B, Niederfriniger Schlag R, Winkler E (2008) Colonization processes on a central alpine glacier foreland. J Veg Sci 19:855–862. https://doi.org/10.3170/2008-8-18464

Erschbamer B, Anich C, Benirschke M, Ganthaler A, Grassmair R, Hasibeder R, Huter V, Konzett D, Lechleitner M, Magauer M, Miller R, Newerkla S, Schneider J, Zeisler B, Schwienbacher E (2010) Das Keimverhalten von 13 alpinen Arten der Familie Asteraceae im Licht und im Dunkeln. Ber Nat-Med Verein Innsbruck 96:73–78

Fenner M, Thompson K (2005) The ecology of seeds, 1st edn. Cambridge University Press, Cambridge

Fernández-Pascual E, Jiménez-Alfaro B, Bueno A (2017) Comparative seed germination traits in alpine and subalpine grasslands: higher elevations are associated with warmer germination temperatures. Plant Biol 19:32–40. https://doi.org/10.1111/plb.12472

Finch-Savage WE, Leubner-Metzger G (2006) Seed dormancy and the control of germination. New Phytol 171:501–523. https://doi.org/10.1111/j.1469-8137.2006.01787.x

Fischer MA, Oswald K, Adler W (2008) Exkursionsflora von Österreich, Liechtenstein und Südtirol. Biologiezentrum der Oberösterreichischen Landesmuseen, 3rd edn. Land Oberösterreich, Linz

Flüeler RP (2011) Experimentelle Untersuchungen über Keimung und Etablierung von alpinen Leguminosen. Diss Veröff Geobt Inst ETH Stift Rübel Zürich. https://doi.org/10.3929/ethz-a-000643314

Forbis TA (2003) Seedling demography in an Alpine ecosystem. Am J Bot 90:1197–1206. https://doi.org/10.3732/ajb.90.8.1197

Forbis TA, Diggle PK (2001) Subnivean embryo development in the alpine herb Caltha leptosepala (Ranunculaceae). Can J Bot 79:635–642. https://doi.org/10.1139/b01-037

Frattaroli AR, Di Martino L, Di Cecco V, Catoni R, Varone L, Di Santo M, Gratani L (2013) Seed germination capability of four endemic species in the Central Apennines (Italy): relationships with seed size. Lazaroa 34:43–53. https://doi.org/10.5209/rev_LAZA.2013.v34.n1.42253

García-Fernández A, Escudero A, Lara-Romero C, Iriondo JM (2015) Effects of the duration of cold stratification on early life stages of the Mediterranean alpine plant Silene ciliata. Plant Biol 17:344–350. https://doi.org/10.1111/plb.12226

Giménez-Benavides L, Milla R (2013) Comparative germination ecology of two altitudinal vicariant Saxifraga species endemic to the north of Spain. Plant Biol 15:593–600. https://doi.org/10.1111/j.1438-8677.2012.00663.x

Giménez-Benavides L, Escudero A, Pérez-García F (2005) Seed germination of high mountain Mediterranean species: altitudinal, interpopulation and interannual variability. Ecol Res 20:433–444. https://doi.org/10.1007/s11284-005-0059-4

Gobiet A, Kotlarski S, Beniston M, Heinrich G, Rajczak J, Stoffel M (2014) 21st century climate change in the European Alps-a review. Sci Total Environ 493:1138–1151. https://doi.org/10.1016/j.scitotenv.2013.07.050

Graae BJ, Alsos IG, Ejrnaes R (2008) The impact of temperature regimes on development, dormancy breaking and germination of dwarf shrub seeds from arctic, alpine and boreal sites. Plant Ecol 198:275–284. https://doi.org/10.1007/s11258-008-9403-4

Graae BJ, Ejrnæs R, Lang SI, Meineri E, Ibarra PT, Bruun HH (2011) Strong microsite control of seedling recruitment in tundra. Oecologia 166:565–576. https://doi.org/10.1007/s00442-010-1878-8

Grime JP (1979) Plant strategies and vegetation processes. Wiley, Chichester

Grosjean P, Ibanez Frederic, Etienne M (2018) Package ‘pastecs’: package for analysis of space-time ecological series. https://cran.r-project.org/web/packages/pastecs/pastecs.pdf. Accessed 14 Nov 2019

Grubb PJ (1977) The maintenance of species-richness in plant communities: the importance of the regeneration niche. Biol Rev 52:107–145. https://doi.org/10.1111/j.1469-185x.1977.tb01347.x

Harper JL (1977) Population biology of plants. Academic Press, London

Isselin-Nondedeu F, Bédécarrats A (2013) Germination and seedling responses of subalpine plants to different soil substrates. Folia Geobot 48:39–53. https://doi.org/10.1007/s12224-012-9136-y

Jiménez-Alfaro B, Silveira FAO, Fidelis A, Poschlod P, Commander LE (2016) Seed germination traits can contribute better to plant community ecology. J Veg Sci 27:637–645. https://doi.org/10.1111/jvs.12375

Kawecki TJ, Ebert D (2004) Conceptual issues in local adaptation. Ecol Lett 7:1225–1241. https://doi.org/10.1111/j.1461-0248.2004.00684.x

Körner C (2003) Alpine plant life. Functional plant ecology of high mountain ecosystems. Springer, Berlin

Landolt E, Bäumler B, Erhardt A, Hegg O, Klötzli F, Lämmler W, Nobis M, Rudmann-Maurer K, Schweingruber FH, Theurillat J-P, Urmi E, Vust M, Wohlgemuth T (2010) Flora indicativa. Ecological indicator values and biological attributes of the Flora of Switzerland and the Alps, 2nd edn. Haupt, Bern

Liu K, Baskin JM, Baskin CC, Bu H, Du G, Ma M (2013) Effect of diurnal fluctuating versus constant temperatures on germination of 445 species from the Eastern Tibet Plateau. PLoS ONE. https://doi.org/10.1371/journal.pone.0069364

Marcante S, Winkler E, Erschbamer B (2009) Population dynamics along a primary succession gradient: do alpine species fit into demographic succession theory? Ann Bot 103:1129–1143. https://doi.org/10.1093/aob/mcp047

Margreiter V, Walde J, Erschbamer B (in review) Germination and seedling recruitment of alpine species in a two-year field experiment along an elevation gradient

Milbau A, Graae BJ, Shevtsova A, Nijs I (2009) Effects of a warmer climate on seed germination in the subarctic. Ann Bot 104:287–296. https://doi.org/10.1093/aob/mcp117

Milbau A, Vandeplas N, Kockelbergh F, Nijs I (2017) Both seed germination and seedling mortality increase with experimental warming and fertilization in a subarctic tundra. AoB Plants 9:1–13. https://doi.org/10.1093/aobpla/plx040

Moles AT, Westoby M (2006) Seed size and plant strategy across the whole life cycle. Oikos 113:91–105. https://doi.org/10.1111/j.0030-1299.2006.14194.x

Mondoni A, Daws MI, Belotti J, Rossi G (2009) Germination requirements of the alpine endemic Silene elisabethae Jan: effects of cold stratification, light and GA3. Seed Sci Technol 37:79–87. https://doi.org/10.15258/sst.2009.37.1.10

Mondoni A, Probert RJ, Rossi G, Vegini E, Hay FR (2011) Seeds of alpine plants are short lived: Implications for long-term conservation. Ann Bot 107:171–179. https://doi.org/10.1093/aob/mcq222

Mondoni A, Orsenigo S, Müller JV, Carlsson-Graner U, Jiménez-Alfaro B, Abeli T (2018) Seed dormancy and longevity in subarctic and alpine populations of Silene suecica. Alp Bot 128:71–81. https://doi.org/10.1007/s00035-017-0194-x

Mondoni A, Rossi G, Orsenigo S, Probert RJ (2012) Climate warming could shift the timing of seed germination in alpine plants. Ann Bot 110:155–164. https://doi.org/10.1093/aob/mcs097

Müller JV, Berg C, Détraz-Méroz J, Erschbamer B, Fort N, Lambelet-Haueter C, Margreiter V, Mombrial F, Mondoni A, Pagitz K, Porro F, Rossi G, Schwager P, Breman E (2017) The alpine seed conservation and research network—a new initiative to conserve valuable plant species in the European Alps. J Mt Sci 14:806–810. https://doi.org/10.1007/s11629-016-4313-8

Orsenigo S, Abeli T, Rossi G, Bonasoni P, Pasquaretta C, Gandini M, Mondoni A (2015) Effects of autumn and spring heat waves on seed germination of high mountain plants. PLoS ONE. https://doi.org/10.1371/journal.pone.0133626

Pemadasa MA, Lovell PH (1975) Factors controlling germination of some dune annuals. J Ecol 63:41–59

Pierce S, Bottinelli A, Bassani I, Ceriani RM, Cerabolini BEL (2014) How well do seed production traits correlate with leaf traits, whole-plant traits and plant ecological strategies? Plant Ecol 215:1351–1359. https://doi.org/10.1007/s11258-014-0392-1

Porro F, Tomaselli M, Abeli T, Gandini M, Gualmini M, Orsenigo S, Petraglia A, Rossi G, Carbognani M (2019) Could plant diversity metrics explain climate-driven vegetation changes on mountain summits of the GLORIA network? Biodivers Conserv 28:3575–3596. https://doi.org/10.1007/s10531-019-01837-1

R Core Team (2020) A language and environment for statistical computing. In: R Found. Stat. Comput. https://www.r-project.org. Accessed 15 May 2020

Rosbakh S, Poschlod P (2015) Initial temperature of seed germination as related to species occurrence along a temperature gradient. Funct Ecol 29:5–14. https://doi.org/10.1111/1365-2435.12304

RStudio RsT (2016) Integrated development for R. RStudio. In: RStudio, Inc., Boston, MA. https://www.rstudio.com/. Accessed 15 May 2020

Schütz M (1988) Genetisch-ökologische Untersuchungen an alpinen Pflanzenarten auf verschiedenen Gesteinsunterlagen : Keimungs- und Aussaatversuche = Genetic-ecological studies in alpine plants from various substrata : germination trials and sowing experiments. Veröffentlichungen des Geobot Institutes der Eidg Tech Hochschule, Stift Rübel Zürich, pp 963027–963032

Schütz W, Milberg P, Schutz W (1997) Seed dormancy in carex canescens: regional differences and ecological consequences. Oikos 78:420. https://doi.org/10.2307/3545604

Schwager P, Berg C (2019) Global warming threatens conservation status of alpine EU habitat types in the European Eastern Alps. Reg Environ Chang 19:2411–2421. https://doi.org/10.1007/s10113-019-01554-z

Schwienbacher E, Erschbamer B (2001) Longevity of seeds in a glacier foreland of the Central Alps-a burial experiment. Bull Geobot Inst ETH 68:63–71. https://doi.org/10.5169/seals-377848

Schwienbacher E, Navarro-Cano JA, Neuner G, Erschbamer B (2011) Seed dormancy in alpine species. Flora Morphol Distrib Funct Ecol Plants 206:845–856. https://doi.org/10.1016/j.flora.2011.05.001

Schwienbacher E, Navarro-Cano JA, Neuner G, Erschbamer B (2012) Correspondence of seed traits with niche position in glacier foreland succession. Plant Ecol 213:371–382. https://doi.org/10.1007/s11258-011-9981-4

Shevtsova A, Graae BJ, Jochum T, Milbau A, Kockelbergh F, Beyens L, Nijs I (2009) Critical periods for impact of climate warming on early seedling establishment in subarctic tundra. Glob Chang Biol 15:2662–2680. https://doi.org/10.1111/j.1365-2486.2009.01947.x

Shimono Y, Kudo G (2003) Intraspecific variations in seedling emergence and survival of Potentilla matsumurae (Rosaceae) between alpine fellfield and snowbed habitats. Ann Bot 91:21–29. https://doi.org/10.1093/aob/mcg002

Stöcklin J, Bäumler E (1996) Seed rain, seedling establishment and clonal growth strategies on a glacier foreland. J Veg Sci 7:45–56. https://doi.org/10.2307/3236415

Thompson K, Gastonn KJ, Band SR (1999) Range size, dispersal and niche breadth in the herbaceous flora of central England. J Ecol 87:150–155. https://doi.org/10.1046/j.1365-2745.1999.00334.x

Threadgill PF, Baskin JM, Baskin CC (1981) Dormancy in seeds of Frasera caroliniensis (Gentianaceae). Am J Bot 68:80–86. https://doi.org/10.1002/j.1537-2197.1981.tb06358.x

Tilman D (1994) Competition and biodiversity in spatially structured habitats. Ecology 75:2–16. https://doi.org/10.2307/1939377

Tudela-Isanta M, Fernández-Pascual E, Wijayasinghe M, Orsenigo S, Rossi G, Pritchard HW, Mondoni A (2018) Habitat-related seed germination traits in alpine habitats. Ecol Evol 8:150–161. https://doi.org/10.1002/ece3.3539

Tudela-Isanta M, Ladouceur E, Wijayasinghe M, Pritchard HW, Mondoni A (2018) The seed germination niche limits the distribution of some plant species in calcareous or siliceous alpine bedrocks. Alp Bot 128:83–95. https://doi.org/10.1007/s00035-018-0199-0

Vandelook F, Bolle N, Van Assche JA (2009) Morphological and physiological dormancy in seeds of aegopodium podagraria (apiaceae) broken successively during cold stratification. Seed Sci Res 19:115–123. https://doi.org/10.1017/S0960258509301075

Venables WN, Ripley BD (2002) Modern applied statistics with S, 4th edn. Springer, Berlin

Venn S, Pickering C, Green K (2014) Spatial and temporal functional changes in alpine summit vegetation are driven by increases in shrubs and graminoids. AoB Plants. https://doi.org/10.1093/aobpla/plu008

Vera ML (1997) Effects of altitude and seed size on germination and seedling survival of heathland plants in north spain. Plant Ecol 133:101–106. https://doi.org/10.1023/A:1009729201384

Walder T, Erschbamer B (2015) Temperature and drought drive differences in germination responses between congeneric species along altitudinal gradients. Plant Ecol 216:1297–1309. https://doi.org/10.1007/s11258-015-0509-1

Wang JH, Baskin CC, Chen W, Du GZ (2010) Variation in seed germination between populations of five sub-alpine woody species from eastern Qinghai-Tibet Plateau following dry storage at low temperatures. Ecol Res 25:195–203. https://doi.org/10.1007/s11284-009-0643-0

Wenk EH, Dawson TE (2007) Interspecific differences in seed germination, establishment, and early growth in relation to preferred soil type in an alpine community. Arctic Antarct Alp Res 39:165–176. https://doi.org/10.1657/1523-0430(2007)39[165:IDISGE]2.0.CO;2

Westoby M (1998) A leaf-height-seed (LHS) plant ecology strategy scheme. Plant Soil 199:213–227. https://doi.org/10.1023/A:1004327224729

Wickham H (2017) Package ‘tidyverse’. In: CRAN repos. https://tidyverse.org. Accessed 15 May 2020

Wickham H (2018a) Package ‘reshape’ flexibly reshape data. https://had.co.nz/reshape/. Accessed 15 May 2020

Wickham H (2018b) Package ‘scales’—scale functions for visualization. In: CRAN Repos. https://cran.r-project.org/web/packages/scales/scales.pdf. Accessed 15 May 2020

Wickham H, Winston C (2019) create elegant data visualisations using the grammar of graphics. In: Packag. ‘ggplot2’. https://cran.r-project.org/web/packages/ggplot2/ggplot2.pdf. Accessed 15 May 2020

Winkler E, Marcante S, Erschbamer B (2015) Demography of the alpine pioneer species Saxifraga aizoides in different successional stages at the glacier fore-land of the Rotmoosferner (Obergurgl, ötztal, Austria). Tuexenia 35:267–283. https://doi.org/10.14471/2015.35.002

ZAMG (2016) Jahresbericht/Annual report. https://www.zamg.ac.at/cms/de/topmenu/ueber-uns/jahresberichte. Accessed 29 June 2020

ZAMG (2017) Jahresbericht/Annual report. https://www.zamg.ac.at/cms/de/topmenu/ueber-uns/jahresberichte. Accessed 29 June 2020

ZAMG (2018) Jahresbericht/Annual report. https://www.zamg.ac.at/cms/de/topmenu/ueber-uns/jahresberichte. Accessed 29 June 2020