Abstract
Functional plant traits are used in ecology to explain population dynamics in time and space. However, because the germination niche is an essential stage in alpine plant life cycles and is under strong environmental pressure, we hypothesised that inter-specific variability in germination traits might contribute to alpine plant distributions. Germination traits of seven closely related species from calcareous and siliceous habitats were characterised in the laboratory, including base, optimum and ceiling temperatures (Tb, To, Tc, respectively), base water-potential (Ψb) and the pH range of the germination phenotype. Species’ vegetative traits (specific leaf area, leaf area and leaf dry matter content) were obtained from the TRY-database. Traits and habitat similarities and dissimilarities were assessed. Species were plotted in a multivariate space using two separate principal component analyses: one each for germination and vegetative traits. Species from calcareous habitats showed significantly higher Tb, lower Ψb and lower capacity to germinate under acidic pH than species from siliceous habitats. Moreover, high To and Tc, a narrow temperature range for germination at dispersal, and vegetative traits values were similar across both habitats. Whilst plant traits seem to have adapted to the shared environmental conditions of the two alpine habitats, some germination traits were affected by the habitat differences. In conclusion, species occurrence in two habitats (calcareous, siliceous) appears to be limited by some germination constraints and provide greater differentiation of species habitat preference than that defined by vegetative traits.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abedi M, Bartelheimer M, Poschlod P (2013) Aluminium toxic effects on seedling root survival affect plant composition along soil reaction gradients—a case study in dry sandy grasslands. J Veg Sci 24:1074–1085. https://doi.org/10.1111/jvs.12016
Aeschimann D, Lauber K, Moser DM, Theurillat GP (2004) Flora alpina. Zanichelli, Bologna
Baskin CC, Baskin JM (2014) Ecology, biogeography, and evolution of dormancy and germination
Bastos LLS, Ferraz IDK, Junior MJVL., Pritchard HW (2017) Variation in limits to germination temperature and rates across the seed-seedling transition in the palm Oenocarpus batauafrom the Brazilian Amazon. Seed Sci Technol 45:1–13. https://doi.org/10.15258/sst.2017.45.1.05
Billings WD, Mooney HA (1968) The ecology of artic and alpine plants. Biol Rev 43:481–529. https://doi.org/10.1111/j.1469-185X.1968.tb00968.x
Bradford KJ (2002) Applications of hydrothermal time to quantifying and modeling seed germination and dormancy. Weed Sci 50:248–260. https://doi.org/10.1614/0043-1745(2002)050[0248:AOHTTQ]2.0.CO;2
Burghardt LT, Metcalf CJE, Wilczek AM et al (2015) Modeling the influence of genetic and environmental variation on the expression of plant life cycles across landscapes. Am Nat 185:212–227. https://doi.org/10.1086/679439
Burnham KP, Anderson DR, Huyvaert KP (2011) AIC model selection and multimodel inference in behavioral ecology: some background,observations, and comparisons. Behav Ecol Sociobiol 65:23–35. https://doi.org/10.1007/s00265-010-1029-6
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
Chapman HD (1965) Cation exchange capacity. In: Black CA (ed) Methods of soil analysis—chemical and microbiological properties. Agronomy 9:pp 891–901
Clarkson DT (1969) Metabolic aspects of aluminum toxicity and some possible mechanisms for resistance. In: Rorison I (ed) Ecological aspects for the mineral nutrition of plants, 1st edn. Blackwell Scientific, Oxford, pp 381–397
Covell S, Ellis RH, Roberts EH, Summerfield RJ (1986) The influence of temperature on seed germination rate in grain legumes. I. A comparison of chickpea, lentil, soyabean and cowpea at constant temperatures. J Exp Bot 37:705–715
de Bello F, Price JN, Münkemüller T et al (2012) Functional species pool framework to test for biotic effects on community assembly. Ecology 93:2263–2273. https://doi.org/10.1890/11-1394.1
De Vitis M, Seal CE, Ulian T et al (2014) Rapid adaptation of seed germination requirements of the threatened Mediterranean species Malcolmia littorea(Brassicaceae) and implications for its reintroduction. S Afr J Bot 94:46–50. https://doi.org/10.1016/j.sajb.2014.05.008
Diaz S, Cabido M (2001) Vive la difference: plant functional diversity matters to ecosystem processes. Trends Ecol Evol 16:646–655. https://doi.org/10.1016/S0169-5347(01)02283-2
Díaz S, Kattge J, Cornelissen JHC et al (2015) The global spectrum of plant form and function. Nature 529:167–171. https://doi.org/10.1038/nature16489
Donohue K, Rubio de Casas R, Burghardt L et al (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
Dürr C, Dickie JB, Yang X-Y, Pritchard HW (2015) Ranges of critical temperature and water potential values for the germination of species worldwide: contribution to a seed trait database. Agric For Meteorol 200:222–232. https://doi.org/10.1016/j.agrformet.2014.09.024
Eriksson O, Bolmgren K, Westin A, Lennartsson T (2015) Historic hay cutting dates from Sweden 1873–1951 and their implications for conservation management of species-rich meadows. Biol Conserv 184:100–107. https://doi.org/10.1016/j.biocon.2015.01.012
European Commission (2007) The interpretation manual of European Union habitats. European Commission, Brussels
Fenner M, Thompson K (2005) The ecology of seeds. Cambridge University Press, Cambridge
Fernández-Pascual E, Jiménez-Alfaro B, Hájek M et al (2015) Soil thermal buffer and regeneration niche may favour calcareous fen resilience to climate change. Folia Giobot. https://doi.org/10.1007/s12224-015-9223-y
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
Fraaije RGA, ter Braak CJF, Verduyn B et al (2015) Early plant recruitment stages set the template for the development of vegetation patterns along a hydrological gradient. Funct Ecol 29:971–980. https://doi.org/10.1111/1365-2435.12441
Funk JL, Larson JE, Ames GM et al (2016) Revisiting the Holy Grail: using plant functional traits to understand ecological processes. Biol Rev 92:1156–1173. https://doi.org/10.1111/brv.12275
García-Huidobro J, Monteith JL, Squire GR (1982) Time, temperature and germination of pearl millet (Pennisetum typhoidesS. & H.). J Exp Bot 33:288–296. https://doi.org/10.1093/jxb/33.2.288
Giménez-Benavides L, Milla R (2013) Comparative germination ecology of two altitudinal vicariant Saxifragaspecies 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(4):433–444
Giménez-Benavides L, Escudero A, Iriondo JM (2007) Local adaptation enhances seedling recruitment along an altitudinal gradient in a high mountain Mediterranean plant. Ann Bot 99:723–734. https://doi.org/10.1093/aob/mcm007
Graham EA, Lam Y, Yuen EM (2010) Forest understory soil temperatures and heat flux calculated using a Fourier model and scaled using a digital camera. Agric For Meteorol 150:640–649. https://doi.org/10.1016/j.agrformet.2010.02.005
Graham EA, Rundel PW, Kaiser W et al (2012) Fine-scale patterns of soil and plant surface temperatures in an alpine fellfield habitat, White Mountains, California. Arct Antarct Alp Res 44:288–295. https://doi.org/10.1657/1938-4246-44.3.288
Grime JP (1977) Evidence for the existence of three primary strategies in plants and its relevance to ecological and evolutionary theory. Am Nat 111(982):1169–1194
Grime JP (2002) Plant strategies, vegetation processes, and ecosystem properties. Wiley, Hoboken
Gross N, Liancourt P, Butters R et al (2015) Functional equivalence, competitive hierarchy and facilitation determine species coexistence in highly invaded grasslands. New Phytol 206:175–186. https://doi.org/10.1111/nph.13168
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
Gummerson RJ (1986) The effect of constant temperatures and osmotic potentials on the grmination of sugar beet. J Exp Bot 41:1431–1439. https://doi.org/10.1093/jxb/37.6.729
Hardegree SP, Moffet CA, Flerchinger GN et al (2013) Hydrothermal assessment of temporal variability in seedbed microclimate. Rangel Ecol Manag 66:127–135. https://doi.org/10.2111/REM-D-11-00074.1
Hofmann K, Farbmacher S, Illmer P (2016) Methane flux in montane and subalpine soils of the Central and Northern Alps. Geoderma 281:83–89. https://doi.org/10.1016/j.geoderma.2016.06.030
Hoyle GL, Steadman KJ, Good RB et al (2015) Seed germination strategies: an evolutionary trajectory independent of vegetative functional traits. Front Plant Sci 6:731. https://doi.org/10.3389/fpls.2015.00731
Huang Z, Liu S, Bradford KJ et al (2016) The contribution of germination functional traits to population dynamics of a desert plant community. Ecol 97:250–261. https://doi.org/10.1890/15-0744.1
Hutchinson GE (1957) Cold Spring Harbor symposium on quantitative biology
Jiménez-Alfaro B, Silveira FAO, Fidelis A et al (2016) Seed germination traits can contribute better to plant community ecology. J Veg Sci 27:637–645. https://doi.org/10.1111/jvs.12375
Kammer PM, Möhl A (2002) Factors controlling species richness in alpine plant communities: an assessment of the importance of stress and disturbance. Arct Antarct Alp Res 34:398. https://doi.org/10.2307/1552197
Kattge J, Diaz S, Lavorel S et al (2011) TRY –a global database of plant traits. Glob Chang Biol 17:2905–2935. https://doi.org/10.1111/J.1365-2486.2011.02451.X
Keddy PA (1992) Assembly and response rules: two goals for predictive community ecology. J Veg Sci 3:157–164. https://doi.org/10.2307/3235676
Körner C (2003) Alpine plant life: functional plant ecology of high mountain ecosystems. Springer, Berlin
Larson JE, Funk JL (2016) Regeneration: an overlooked aspect of trait-based plant community assembly models. J Ecol 104:1284–1298. https://doi.org/10.1111/1365-2745.12613
Laughlin DC (2014) Applying trait-based models to achieve functional targets for theory-driven ecological restoration. Ecol Lett 17:771–784. https://doi.org/10.1111/ele.12288
Lê S, Rennes A, Josse J, Husson F (2008) FactoMineR: an R package for multivariate analysis. J Stat Softw. https://doi.org/10.18637/jss.v025.i01
McGill B, Enquist B, Wether E, WESTOBY M (2006) Rebuilding community ecology from functional traits. Trends Ecol Evol 21:178–185. https://doi.org/10.1016/j.tree.2006.02.002
McKee J, Richards AJ (1996) Variation in seed production and germinability in common reed (Phragmites australis) in Britain and France with respect to climate. New Phytol 133:233–243. https://doi.org/10.1111/j.1469-8137.1996.tb01890.x
Merritt DJ, Dixon KW, Nelleman C et al (2011) Restoration seed banks—a matter of scale. Science 332:424–425. https://doi.org/10.1126/science.1203083
Michel B (1983) The evaluation ofwater potentials of solutions of polyethylene glycol 8000 both in the absence and presence of other solutes. Plant Physiol 72:739–742
Nagy L, Grabherr G (2009) The biology of alpine habitats. Oxford University Press, Oxford
Nguyen H, Firn J, Lamb D, Herbohn J (2014) Wood density: a tool to find complementary species for the design of mixed species plantations. For Ecol Manag 334:106–113. https://doi.org/10.1016/j.foreco.2014.08.022
Ordoñez-Salanueva CA, Seal CE, Pritchard HW et al (2015) Cardinal temperatures and thermal time in PolaskiaBackeb (Cactaceae) species: effect of projected soil temperature increase and nurse interaction on germination timing. J Arid Environ 115:73–80. https://doi.org/10.1016/j.jaridenv.2015.01.006
Orru M, Mattana E, Pritchard HW, Bacchetta G (2012) Thermal thresholds as predictors of seed dormancy release and germination timing:altitude-related risks from climate warming for the wild grapevine Vitis viniferasubsp. sylvestris. Ann Bot 110:1651–1660. https://doi.org/10.1093/aob/mcs218
Orsenigo S, Abeli T, Rossi G et al (2015) Effects of autumn and spring heat waves on seed germination of high mountain plants. PLoS One 10:1–17. https://doi.org/10.1371/journal.pone.0133626
Pierce S, Negreiros D, Cerabolini BEL et al (2017) A global method for calculating plant CSR ecological strategies applied across biomes world-wide. Funct Ecol 31:444–457. https://doi.org/10.1111/1365-2435.12722
Poorter L, Wright SJ, Paz H et al (2008) Are functional traits good predictors of demographic rates? Evidence from five neotropical forests. Ecology 89:1908–1920. https://doi.org/10.1890/07-0207.1
Porceddu M, Mattana E, Pritchard HW, Bacchetta G (2013) Thermal niche for in situ seed germination by Mediterranean mountain streams: model prediction and validation for Rhamnus persicifoliaseeds. Ann Bot 112:1887–1897. https://doi.org/10.1093/aob/mct238
Poschlod P, Abedi M, Bartelheimer M et al (2013) Seed ecology and assembly rules in plant communities. In: van der Maarel E, Franklin J (eds) Vegetation ecology, 2nd edn. pp 164–202
Read QD, Moorhead LC, Swenson NG et al (2014) Convergent effects of elevation on functional leaf traits within and among species. Funct Ecol 28:37–45. https://doi.org/10.1111/1365-2435.12162
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
Schmidtlein S, Feilhauer H, Bruelheide H (2012) Mapping plant strategy types using remote sensing. J Veg Sci 23:395–405. https://doi.org/10.1111/j.1654-1103.2011.01370.x
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
Seal CE, Daws MI, Flores J et al (2017) Thermal buffering capacity of the germination phenotype across the environmental envelope of the Cactaceae. Glob Chang Biol. https://doi.org/10.1111/gcb.13796
Shimono Y, Kudo G (2005) Comparisons of germination traits of alpine plants between fellfield and snowbed habitats. Ecol Res 20:189–197. https://doi.org/10.1007/s11284-004-0031-8
Sommerville KD, Martyn AJ, Offord CA (2013) Can seed characteristics or species distribution be used to predict the stratification requirements of herbs in the Australian Alps? Bot J Linn Soc 172:187–204. https://doi.org/10.1111/boj.12021
Tudela-Isanta M, Fernández-Pascual E, Wijayasinghe M, Orsenigo S, Pritchard WH, Rossi G, Mondoni A (2017) Habitat-related seed germination traits in alpine habitats. Ecol Evol (in press)
Valladares F, Matesanz S, Guilhaumon F et al (2014) The effects of phenotypic plasticity and local adaptation on forecasts of species range shifts under climate change. Ecol Lett 17:1351–1364. https://doi.org/10.1111/ele.12348
Venn SE, Green K, Pickering CM, Morgan JW (2011) Using plant functional traits to explain community composition across a strong environmental filter in Australian alpine snowpatches. Plant Ecol 212:1491–1499. https://doi.org/10.1007/s11258-011-9923-1
Walder T, Erschbamer B (2015) Temperature and drought drive differences in germination responses between congeneric species along altitudinal gradients. Plant Ecol 216:1297–1309
Wilczek AM, Roe JL, Knapp MC et al (2009) Effects of genetic perturbation on seasonal life history plasticity. Science 323(5916):930–934. https://doi.org/10.1126/science.1165826
Wright IJ, Reich PB, Westoby M et al (2004) The worldwide leaf economics spectrum. Nature 428:821–827. https://doi.org/10.1038/nature02403
Acknowledgements
The research leading to these results received funding from thePeople Programme (Marie Curie Actions) of the European Union’s SeventhFramework Programme FP7/2007–2013/ under REA Grant Agreement No. 607785. The Royal Botanic Gardens, Kew receives grant-in-aid from Defra.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that we have no conflict of interest.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Tudela-Isanta, M., Ladouceur, E., Wijayasinghe, M. et al. The seed germination niche limits the distribution of some plant species in calcareous or siliceous alpine bedrocks. Alp Botany 128, 83–95 (2018). https://doi.org/10.1007/s00035-018-0199-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00035-018-0199-0