Skip to main content

Advertisement

Log in

Seed mass and plant home site environment interact to determine alpine species germination patterns along an elevation gradient

  • Original Article
  • Published:
Alpine Botany Aims and scope Submit manuscript

Abstract

Ongoing changes in temperature and precipitation regime may have a strong impact on vulnerable life-history stages such as germination, especially in alpine regions. Differences in germination patterns among species and populations may reflect their adaptation to conditions of their origin or may be determined by the phylogenetic constraints. These two effects are, however, rarely separated. All the germination patterns may also be modified by seed mass. We studied 40 populations of 14 species of Impatiens coming from different elevations in the Himalayas. Three home site temperatures were simulated and one warmer temperature according to a climate change scenario were used. We also studied the combined effect of shorter stratification and warmer temperature as another possible effect of climate change. Interactions of home site and germination conditions affected total germination and germination speed, but not seed dormancy. Seed mass and home site conditions’ interaction indicated different germination strategies in light and heavy seeds. Only seed mass was affected by phylogenetic relationships among the species, while germination response (except T30) was driven primarily by home site conditions. This study is the first to show that the effect of seed mass interacts with home site conditions in determining species’ germination patterns under changing climate. The differences in seed mass are thus likely crucial for species’ ability to adapt to novel conditions since seed mass, unlike seed germination patterns, is strongly phylogenetically constrained. Further studies exploring how seed mass modifies species’ germination under changing climate are needed to confirm generalisability of these findings.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Data availability

All data generated or analysed during this study are included in this published in supplementary information files [ESM_5–Data].

References

  • Ackerly DD, Donoghue MJ (1995) Phylogeny and ecology reconsidered. J Ecol 83:730–733

    Google Scholar 

  • Aragon-Gastelum J, Badano E, Yanez-Espinosa L, Ramirez-Tobias HM, Rodas-Ortiz JP, Gonzalez-Salvatierra C, Flores J (2017) Seedling survival of three endemic and threatened Mexican cacti under induced climate change. Plant Species Biol 32:92–99

    Google Scholar 

  • Association of official seed analysts officers and committees for 1983–1984 (1984) Seed Sci Technol 2:162–164

    Google Scholar 

  • Barak RS, Lichtenberger TM, Wellman-Houde A, Kramer AT, Larkin DJ (2018) Cracking the case: seed traits and phylogeny predict time to germination in prairie restoration species. Ecol Evol 8:5551–5562

    PubMed  PubMed Central  Google Scholar 

  • Baskin CC, Baskin JM (1988) Germination ecophysiology of herbaceous plant-species in a temperate region. Am J Bot 75:286–305

    Google Scholar 

  • Baskin JM, Baskin CC, Parr JC (1986) Field emergence on Lamium amplexicaule L. and Lamium purpureum L. in relation to the annual seed dormancy cycle. Weed Res 26:185–190

    Google Scholar 

  • Baskin CC, Baskin JM (2014) Seeds: ecology, biogeography, and evolution of dormancy and germination, 2nd edn. Academic Press, San Diego

    Google Scholar 

  • Bates D, Machler M, Bolker BM, Walker SC (2015) Fitting linear mixed-effects models using lme4. J Stat Soft 67:1–48

    Google Scholar 

  • Bauk K, Flores J, Ferrero C, Perez-Sanchez R, Penas MLL, Gurvich DE (2017) Germination characteristics of Gymnocalycium monvillei (Cactaceae) along its entire altitudinal range. Botany 95:419–428

    Google Scholar 

  • Benech-Arnold R, Sánchez R (2004) Handbook of seed physiology: applications to agriculture. Food Products Press, New York

    Google Scholar 

  • Beniston M (2012) Is snow in the Alps receding or disappearing? Wiley Interdiscip Rev Clim Change 3:349–358

    Google Scholar 

  • Briceno VF, Hoyle GL, Nicotra AB (2015) Seeds at risk: how will a changing alpine climate affect regeneration from seeds in alpine areas? Alp Bot 125:59–68

    Google Scholar 

  • Bu HY, Du GZ, Chen XL, Xu XL, Liu K, Wen SJ (2008) Community-wide germination strategies in an alpine meadow on the eastern Qinghai-Tibet plateau: phylogenetic and life-history correlates. Plant Ecol 195:87–98

    Google Scholar 

  • Butler CJ, Wheeler EA, Stabler LB (2012) Distribution of the threatened lace hedgehog cactus (Echinocereus reichenbachii) under various climate change scenarios. J Torrey Bot Soc 139:46–55

    Google Scholar 

  • Carta A, Hanson S, Muller JV (2016a) Plant regeneration from seeds responds to phylogenetic relatedness and local adaptation in Mediterranean Romulea (Iridaceae) species. Ecol Evol 6:4166–4178

    PubMed  PubMed Central  Google Scholar 

  • Carta A, Probert R, Moretti M, Peruzzi L, Bedini G (2014) Seed dormancy and germination in three Crocus ser. rerni species (Iridaceae): implications for evolution of dormancy within the genus. Plant Biol 16:1065–1074

    CAS  PubMed  Google Scholar 

  • Carta A, Probert R, Puglia G, Peruzzi L, Bedini G (2016b) Local climate explains degree of seed dormancy in Hypericum elodes L. (Hypericaceae). Plant Biol 18:76–82

    PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Chamorro D, Luna B, Moreno JM (2013) Germination response to various temperature regimes of four Mediterranean seeder shrubs across a range of altitudes. Plant Ecol 214:1431–1441

    Google Scholar 

  • Climate change 2014. Synthesis report. Core writing team, Pachauri RK, Meyer LA (eds) Contribution of working groups I, II and III to the fifth assessment report of the intergovernmental panel on climate change. IPCC, Geneva, Switzerland

  • Coolbear P, Francis A, Grierson D (1984) The effect of low-tempereture pre-sowing treatment on the germination performance and membrane integrity of artificially aged tomato seeds. J Exp Bot 35:1609–1617

    CAS  Google Scholar 

  • Cottrell HJ (1947) Tetrazolium salt as a seed germination indicator. Nature 159:748–748

    CAS  PubMed  Google Scholar 

  • Davila P, Tellez O, Lira R (2013) Impact of climate change on the distribution of populations of an endemic Mexican columnar cactus in the Tehuacan-Cuicatlan Valley, Mexico. Plant Biosyst 147:376–386

    Google Scholar 

  • Dayrell RLC, Garcia QS, Negreiros D, Baskin CC, Baskin JM, Silveira FAO (2017) Phylogeny strongly drives seed dormancy and quality in a climatically buffered hotspot for plant endemism. Ann Bot 119:267–277

    PubMed  Google Scholar 

  • Diniz JAF, De Santana CER, Bini LM (1998) An eigenvector method for estimating phylogenetic inertia. Evolution 52:1247–1262

    Google Scholar 

  • Desdevises Y, Legendre P, Azouzi L, Morand S (2003) Quantifying phylogenetically structured environmental variation. Evolution 57:2647–2652

    PubMed  Google Scholar 

  • Donohue K, de Casas RR, Burghardt L, Kovach K, Willis CG (2010) Germination, postgermination adaptation, and species ecological ranges. Annu Rev Ecol Evol Syst 41:293–319

    Google Scholar 

  • Dostálek T, Rokaya MB, Münzbergová Z (2019) Effects of temperature of plant cultivation on plant palatability modify species response to novel climate. BioRxiv 8:1. https://doi.org/10.1101/841148

    Article  Google Scholar 

  • Dreesen FE, De Boeck HJ, Janssens IA, Nijs I (2014) Do successive climate extremes weaken the resistance of plant communities? An experimental study using plant assemblages. Biogeosciences 11:109–121

    Google Scholar 

  • Esmaeili MM, Sattarian A, Bonis A, Bouzille JB (2009) Ecology of seed dormancy and germination of Carex divisa huds: effects of stratification, temperature and salinity. Int J Plant Prod 3:27–40

    Google Scholar 

  • Farooq M, Basra SMA, Ahmad N, Hafeez K (2005) Thermal hardening: a new seed vigor enhancement tool in rice. J Integr Plant Biol 47:187–193

    Google Scholar 

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

    Google Scholar 

  • Figueroa JA, Armesto JJ (2001) Community-wide germination strategies in a temperate rainforest of Southern Chile: ecological and evolutionary correlates. Aust J Bot 49:411–425

    Google Scholar 

  • Forbis TA, Floyd SK, de Queiroz A (2002) The evolution of embryo size in angiosperms and other seed plants: implications for the evolution of seed dormancy. Evolution 56:2112–2125

    Google Scholar 

  • Gao S, Wang JF, Zhang ZJ, Dong G, Guo JX (2012) Seed production, mass, germinability, and subsequent seedling growth responses to parental warming environment in Leymus chinensis. Crop Pasture Sci 63:87–94

    Google Scholar 

  • Garcia-Fernandez 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

    CAS  PubMed  Google Scholar 

  • Gardarin A, Daurr C, Colbach N (2011) Prediction of germination rates of weed species: relationships between germination speed parameters and species traits. Ecoll Modell 222:626–636

    Google Scholar 

  • Gimenez-Benavides L, Escudero A, Perez-Garcia F (2005) Seed germination of high mountain Mediterranean species: altitudinal, interpopulation and interannual variability. Ecol Res 20:433–444

    Google Scholar 

  • Grime JP, Mason G, Curtis AV, Rodman J, Band SR, Mowforth MAG, Neal AM, Shaw S (1981) A comparative study of germination characteristics in a local flora. J Ecol 69:1017–1059

    Google Scholar 

  • Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A (2005) Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 25:1965–1978

    Google Scholar 

  • Hovenden MJ, Wills KE, Chaplin RE, Schoor JKV, Williams AL, Osanai Y, Newton PCD (2008) Warming and elevated CO(2) affect the relationship between seed mass, germinability and seedling growth in Austrodanthonia caespitosa, a dominant Australian grass. Glob Chang Biol 14:1633–1641

    Google Scholar 

  • Hoyle GL, Venn SE, Steadman KJ, Good RB, McAuliffe EJ, Williams ER, Nicotra AB (2013) Soil warming increases plant species richness but decreases germination from the alpine soil seed bank. Glob Chang Biol 19:1549–1561

    PubMed  Google Scholar 

  • Hradilová I, Duchoslav M, Brus J, Pechanec V, Hýbl M, Kopecký P, Smržová L, Štefelová N, Václavek T, Bariotakis M, Machalová J, Hron K, Pirintsos S, Smykal P (2019) Variation in wild pea (Pisum sativum subsp. elatius) seed dormancy and its relationship to the environment and seed coat traits. PeerJ 7:e6263. https://doi.org/10.7717/peerj.6263

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Janssens SB, Knox EB, Huysmans S, Smets EF, Merckx V (2009) Rapid radiation of Impatiens (Balsaminaceae) during Pliocene and Pleistocene: result of a global climate change. Mol Phylogenet Evol 52:806–824

    CAS  PubMed  Google Scholar 

  • Klady RA, Henry GHR, Lemay V (2011) Changes in high arctic tundra plant reproduction in response to long-term experimental warming. Glob Chang Biol 17:1611–1624

    Google Scholar 

  • Knapp AK, Beier C, Briske DD, Classen AT, Luo Y, Reichstein M, Smith MD, Smith SD, Bell JE, Fay PA, Heisler JL, Leavitt SW, Sherry R, Smith B, Weng E (2008) Consequences of more extreme precipitation regimes for terrestrial ecosystems. Bioscience 58:811–821

    Google Scholar 

  • Leishman MR, Westoby M, Jurado E (1995) Correlates of seed size variation—a comparison among 5 temperate floras. J Ecol 83:517–529

    Google Scholar 

  • Liu K, Baskin JM, Baskin CC, Bu HY, Du GZ, Ma MJ (2013) Effect of diurnal fluctuating versus constant temperatures on germination of 445 species from the Eastern Tibet Plateau. PLoS ONE 8:e69364. https://doi.org/10.1371/journal.pone.0069364

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martin MC (1965) An ecological life history of Geranium maculatum. Am Midl Nat 73:111–149

    Google Scholar 

  • Meyer SE (1992) Habitat correlated variation in Firecracker penstemon (Penstemon eatonii gray-Scrophulariaceae) seed germination response. Bull Torrey Bot Club 119:268–279

    Google Scholar 

  • Meyer SE, Allen PS, Beckstead J (1997) Seed germination regulation in Bromus tectorum (Poaceae) and its ecological significance. Oikos 78:475–485

    Google Scholar 

  • Mira S, Arnal A, Perez-Garcia F (2017) Habitat-correlated seed germination and morphology in populations of Phillyrea angustifolia L. (Oleaceae). Seed Sci Res 27:50–60

    Google Scholar 

  • Moles AT, Ackerly DD, Webb CO, Tweddle JC, Dickie JB, Westoby M (2005) A brief history of seed size. Science 307:576–580

    CAS  PubMed  Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • Münzbergová Z, Hadincová V, Skálová H, Vandvik V (2017) Genetic differentiation and plasticity interact along temperature and precipitation gradients to determine plant performance under climate change. J Ecol 105:1358–1373

    Google Scholar 

  • Münzbergová Z, Plačková I (2010) Seed mass and population characteristics interact to determine performance of Scorzonera hispanica under common garden conditions. Flora 205:552–559

    Google Scholar 

  • Münzbergová Z, Kosová V, Schnáblová R, Rokaya M, Synková H, Haisel D, Wilhelmová N, Dostálek T (2020) Plant origin, but not phylogeny, drive species ecophysiological response to projected climate. Front Plant Sci 11:1–18

    Google Scholar 

  • Navarro L, Guitian J (2003) Seed germination and seedling survival of two threatened endemic species of the northwest Iberian peninsula. Biol Conser 109:313–320

    Google Scholar 

  • Ndihokubwayo N, Nguyen VT, Cheng DD (2016) Effects of origin, seasons and storage under different temperatures on germination of Senecio vulgaris (Asteraceae) seeds. Peerj 4:e2346. https://doi.org/10.7717/peerj.2346

    Article  PubMed  PubMed Central  Google Scholar 

  • Norden N, Daws MI, Antoine C, Gonzalez MA, Garwood NC, Chave J (2009) The relationship between seed mass and mean time to germination for 1037 tree species across five tropical forests. Funct Ecol 23:203–210

    Google Scholar 

  • Ooi MKJ, Auld TD, Denham AJ (2012) Projected soil temperature increase and seed dormancy response along an altitudinal gradient: implications for seed bank persistence under climate change. Plant Soil 353:289–303

    CAS  Google Scholar 

  • Paulů A, Harčariková L, Münzbergová Z (2017) Are there systematic differences in germination between rare and common species? A case study from central European mountains. Flora 236–237:15–24. https://doi.org/10.1007/s11104-012-1584-x

    Article  CAS  Google Scholar 

  • Paradis E, Claude J, Strimmer K (2004) APE: analyses of phylogeneticsand evolution in R language. Bioinformatics 20:289–290. https://doi.org/10.1093/bioinformatics/btg412

    Article  CAS  PubMed  Google Scholar 

  • Pederson GT, Betancourt JL, McCabe GJ (2013) Regional patterns and proximal causes of the recent snowpack decline in the Rocky Mountains. US Geophys Res Lett 40:1811–1816

    Google Scholar 

  • Perglová I, Pergl J, Skalová H, Moravcová L, Jarošík V, Pyšek P (2009) Differences in germination and seedling establishment of alien and native Impatiens species. Preslia 81:357–375

    Google Scholar 

  • Press JR, Shrestha KK, Sutton DA (2000) Annotated checklist of the flowering plants of Nepal. Natural History Museum, London

    Google Scholar 

  • Qaderi MM, Cavers PB (2002) Interpopulation and interyear variation in germination in Scotch thistle, Onopordum acanthium L., grown in a common garden: genetics vs environment. Plant Ecol 162:1–8

    Google Scholar 

  • Rees M, Condit R, Crawley M, Pacala S, Tilman D (2001) Long-term studies of vegetation dynamics. Science 293:650–655

    CAS  PubMed  Google Scholar 

  • Sanchez-Bayo F, Green K (2013) Australian snowpack disappearing under the influence of global warming and solar activity. Arct Antarct Alp Res 45:107–118

    Google Scholar 

  • Santo A, Mattana E, Baechetta G (2015) Inter- and intra-specific variability in seed dormancy loss and germination requirements in the Lavatera triloba aggregate (Malvaceae). Plant Ecol Evol 148:100–110

    Google Scholar 

  • Satyanti A, Guja LK, Nicotra AB (2019) Temperature variability drives within-species variation in germination strategy and establishment characteristics of an alpine herb. Oecologia 189:407–419

    PubMed  Google Scholar 

  • Schütz W, Milberg P (1997) Seed dormancy in Carex canescens: regional differences and ecological consequences. Oikos 78:420–428

    Google Scholar 

  • Schütz W, Rave G (1999) The effect of cold stratification and light on the seed germination of temperate sedges (Carex) from various habitats and implications for regenerative strategies. Plant Ecol 144:215–230

    Google Scholar 

  • Seglias AE, Williams E, Bilge A, Kramer AT (2018) Phylogeny and source climate impact seed dormancy and germination of restoration-relevant forb species. PLoS ONE 13:0191931. https://doi.org/10.1371/journal.pone.0191931

    Article  CAS  Google Scholar 

  • Sevruk B (1997) Regional dependency of precipitation-altitude relationship in the Swiss Alps. Clim Change 36:355–369

    Google Scholar 

  • Song Y, Yuan YM, Kupfer P (2003) Chromosomal evolution in Balsaminaceae, with cytological observations on 45 species from Southeast Asia. Caryologia 56:463–481

    Google Scholar 

  • Soomro AG, Babar MM, Ashraf A, Memon A (2019) The relationship between precipitation and elevation of the watershed in the Khirthar National Range. Mehran Univ Res J Eng Technol 38:1067–1076

    Google Scholar 

  • Tatebe H, Ishii M, Mochizuki T, Chikamoto Y, Sakamoto TT, Komuro Y, Mori M, Yasunaka S, Watanabe M, Ogochi K, Suzuki T, Nishimura T, Kimoto M (2012) The initialization of the MIROC climate models with hydrographic data assimilation for decadal prediction. J Meteorol Soc Japan 90A:275–294

    Google Scholar 

  • Thompson K (1993) Persistence in soil. In: Hendry GAF, Grime JP (eds) Methods in comparative plant ecology: a laboratory manual. Chapman & Hall, London, pp 199–202

    Google Scholar 

  • Tingstad L, Olsen SL, Klanderud K, Vandvik V, Ohlson M (2016) Temperature, precipitation and biotic interactions as determinants of tree seedling recruitment across the tree line ecotone. Oecologia 180:917–918

    PubMed  Google Scholar 

  • Veselá A, Duongová L, Münzbergová Z (2020). Plant origin determines seed mass, seed nutrients and germination behavior of a dominant grass species. https://doi.org/10.1101/2020.03.02.973552

  • Walck JL, Hidayati SN, Dixon KW, Thompson K, Poschlod P (2011) Climate change and plant regeneration from seed. Glob Chang Biol 17:2145–2161

    Google Scholar 

  • Walder T, Erschbamer B (2015) Temperature and drought drive differences in germination responses between congeneric species along altitudinal gradients. Plant Ecol 216:1297–1309

    Google Scholar 

  • Wang JH, Baskin CC, Cui XL, Du GZ (2009) Effect of phylogeny, life history and habitat correlates on seed germination of 69 arid and semi-arid zone species from northwest China. Evol Ecol 23:827–846

    Google Scholar 

  • Wang JH, Chen W, Baskin CC, Baskin JM, Cui XL, Zhang Y, Qiang WY, Du GZ (2012) Variation in seed germination of 86 subalpine forest species from the eastern Tibetan Plateau: phylogeny and life-history correlates. Ecol Res 27:453–465

    Google Scholar 

  • Westoby M, Leishman MR, Lord JM (1995) On misinterpreting the phylogenetic correction. J Ecol 83:531–534

    Google Scholar 

  • Willis CG, Baskin CC, Baskin JM, Auld JR, Venable DL, Cavender-Bares J, Donohue K, de Casas RR, Grp NEGW (2014) The evolution of seed dormancy: environmental cues, evolutionary hubs, and diversification of the seed plants. New Phytol 203:300–309

    PubMed  Google Scholar 

  • Wu GL, Du GZ (2007) Germination is related to seed mass in grasses (Poaceae) of the eastern Qinghai-Tibetan Plateau. China Nord J Bot 25:361–365

    Google Scholar 

  • Wu GL, Li W, Du GZ (2011) Relationship between germination and seed size in alpine shrubs in Tibetan Plateau. Pak J Bot 43:2793–2796

    Google Scholar 

  • Xu J, Li WL, Zhang CH, Liu W, Du GZ (2014) Variation in seed germination of 134 common species on the Eastern Tibetan Plateau: phylogenetic, life history and environmental correlates. PLoS ONE 9:e098601. https://doi.org/10.1371/journal.pone.0098601

    Article  CAS  Google Scholar 

  • Yu SX, Janssens SB, Zhu XY, Liden M, Gao TG, Wang W (2016) Phylogeny of Impatiens (Balsaminaceae): integrating molecular and morphological evidence into a new classification. Cladistics 32:179–197

    Google Scholar 

  • Yuan YM, Song Y, Geuten K, Rahelivololona E, Wohlhauser S, Fischer E, Smets E, Kupfer P (2004) Phylogeny and biogeography of Balsaminaceae inferred from ITS sequences. Taxon 53:391–403

    Google Scholar 

  • Zhang ST, Du GZ, Chen JK (2004) Seed size in relation to phylogeny, growth form and longevity in a subalpine meadow on the east of the Tibetan Plateau. Folia Geobot 39:129–142

    Google Scholar 

Download references

Acknowledgements

We thank Z. Líblová and M. Lokvencová for help with the germination experiment, Z. Líblová and M. Šurinová for providing their unpublished phylogenetic data, Wojciech Adamowski for help with species identification and two anonymous reviewers for helpful comments on the previous version of the manuscript. The study was supported by project GAČR 17-10280S.

Funding

The study was supported by project Grant Agency of Czech Republic 17-10280S.

Author information

Authors and Affiliations

Authors

Contributions

AV, TD, ZM conceived and designed the experiments. MBR conducted the fieldwork and AV performed the germination experiments. AV and ZM analysed the data. AV wrote the manuscript and all authors contributed to the final version of the manuscript.

Corresponding author

Correspondence to Andrea Veselá.

Ethics declarations

Conflict of interest

All authors declare no conflict of interest. All authors agree with this submission.

Ethical approval

We followed the ethical standards.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Veselá, A., Dostálek, T., Rokaya, M.B. et al. Seed mass and plant home site environment interact to determine alpine species germination patterns along an elevation gradient. Alp Botany 130, 101–113 (2020). https://doi.org/10.1007/s00035-020-00242-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00035-020-00242-7

Keywords

Navigation