Abstract
Polyploidy may affect a species’ eco-physiology, which might, in turn, trigger a shift in the distribution of its cytotypes. The arcto-alpine Hieracium alpinum (Asteraceae) encompasses two geographically allopatric cytotypes: diploids occurring in the South-Eastern Carpathians and triploids occupying the remaining, much larger part of the species range. We ask whether the natural populations of these two cytotypes, growing under partially different biotic and abiotic conditions, also differ in selected eco-physiological traits. To answer this question, we analyzed specific leaf area, foliar carbon (C) and nitrogen (N) contents, and their stable isotope compositions in plants sampled in 27 populations across the species range. Our results did not show any differences in these traits, except foliar N content being significantly higher in diploids. This pattern was mostly driven by the Scandinavian triploid populations exposed to significantly lower amounts of solar radiation and precipitation during the growing season when compared to the continental populations. As a consequence, in addition to lower foliar N content, the Scandinavian populations exhibited also lower foliar C content, but higher C/N ratios than continental populations regardless of their cytotype. Across the species range, foliar N and C contents were positively associated with the amount of precipitation, whilst δ15N was positively associated with temperature and negatively with the surrounding species richness and vegetation cover. Significantly lower values of δ13C in Scandinavian populations are likely the effect of increased atmospheric pressure due to the lower elevational position of Scandinavian sites. Reproductive output was positively linked to amounts of foliar nitrogen and δ15N. Our data thus show that (1) the latitudinal-driven abiotic and biotic factors affected eco-physiological traits in significantly larger extent than ploidy level and that (2) continental and Scandinavian populations, though all confined to the alpine belt, considerably differ in their eco-physiology likely reflecting different adaptation strategies.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Amundson R, Austin AT, Schuur EA, Yoo K, Matzek V, Kendall C, Uebersax A, Brenner D, Baisden WT (2003) Global patterns of the isotopic composition of soil and plant nitrogen. Glob Biogeochem Cycles. https://doi.org/10.1029/2002GB001903
Arroyo MTK, Dudley L, Pliscoff P, Cavieres LA, Squeo FA, Marticorena C, Rozzi R (2009) A possible correlation between the altitudinal and latitudinal ranges of species in the high elevation flora of the Andes. In: Spehn EM, Körner C (eds) Data mining for global trends in mountain biodiversity. CRC Press/Taylor and Francis Group, Boca Raton, pp 39–47
Aspelmeier S, Leuschner C (2006) Genotypic variation in drought response of silver birch (Betula pendula Roth): leaf and root morphology and carbon partitioning. Trees 20:42–52. https://doi.org/10.1007/s00468-005-0011-9
Baldwin J (1941) Galax: the genus and its chromosomes. J Hered 32:249–254. https://doi.org/10.1093/oxfordjournals.jhered.a105053
Bales AL (2015) Investigating the role of polyploidy in the response of Chamerion angustifolium to increased soil nitrogen availability and insect herbivory. Master’s thesis, Michigan Technological University
Bates D, Mächler M, Bolker B, Walker S (2014) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48. https://doi.org/10.18637/jss.v067.i01
Bauert MR (1996) Genetic diversity and ecotypic differentiation in arctic and alpine populations of Polygonum viviparum. Arct Alp Res 28:190–195. https://doi.org/10.2307/1551759
Bret-Harte MS, Shaver GR, Chapin FS (2002) Primary and secondary stem growth in arctic shrubs: implications for community response to environmental change. J Ecol 90:251–267. https://doi.org/10.1046/j.1365-2745.2001.00657.x
Brock MT, Galen C (2005) Drought tolerance in the alpine dandelion, Taraxacum ceratophorum (Asteraceae), its exotic congener T. officinale, and interspecific hybrids under natural and experimental conditions. Am J Bot 92:1311–1321. https://doi.org/10.3732/ajb.92.8.1311
Buggs RJ, Pannell JR (2007) Ecological differentiation and diploid superiority across a moving ploidy contact zone. Evolution 61:125–140. https://doi.org/10.1111/j.1558-5646.2007.00010.x
Casper BB, Forseth IN, Kempenich H, Seltzer S, Xavier K (2001) Drought prolongs leaf life span in the herbaceous desert perennial Cryptantha flava. Funct Ecol 15:740–747. https://doi.org/10.1046/j.0269-8463.2001.00583.x
Chrtek J (1997) Taxonomy of the Hieracium alpinum group in the Sudeten Mts., the West and the Ukrainian East Carpathians. Folia Geobot 32:69–97. https://doi.org/10.1007/BF02803888
Compositae (2003) Mentor effects in the genus Hieracium s. str. Lactuceae). Folia Geobot 38:345–350. https://doi.org/10.1007/BF02803204
Craine JM, Elmore AJ, Aidar MP, Bustamante M, Dawson TE, Hobbie EA, Kahmen A, Mack MC, McLauchlan KK, Michelsen A (2009) Global patterns of foliar nitrogen isotopes and their relationships with climate, mycorrhizal fungi, foliar nutrient concentrations, and nitrogen availability. New Phytol 183:980–992. https://doi.org/10.1111/j.1469-8137.2009.02917.x
Craine JM, Brookshire E, Cramer MD, Hasselquist NJ, Koba K, Marin-Spiotta E, Wang L (2015) Ecological interpretations of nitrogen isotope ratios of terrestrial plants and soils. Plant Soil 396:1–26. https://doi.org/10.1007/s11104-015-2542-1
Craufurd P, Wheeler T, Ellis R, Summerfield R, Williams J (1999) Effect of temperature and water deficit on water-use efficiency, carbon isotope discrimination, and specific leaf area in peanut. Crop Sci 39:136–142. https://doi.org/10.2135/cropsci1999.0011183X003900010022x
Dray S, Dufour A-B (2007) The ade4 package: implementing the duality diagram for ecologists. J Stat Softw 22:1–20
Evans JR, Poorter H (2001) Photosynthetic acclimation of plants to growth irradiance: the relative importance of specific leaf area and nitrogen partitioning in maximizing carbon gain. Plant Cell Environ 24:755–767. https://doi.org/10.1046/j.1365-3040.2001.00724.x
Farquhar GD, Ehleringer JR, Hubick KT (1989) Carbon isotope discrimination and photosynthesis. Annu Rev Plant Biol 40:503–537. https://doi.org/10.1146/annurev.pp.40.060189.002443
Fick SE, Hijmans RJ (2017) WorldClim 2: new 1-km spatial resolution climate surfaces for global land areas. Int J Climatol 37:4302–4315. https://doi.org/10.1002/joc.5086
Field C, Mooney H (1986) The photosynthesis–nitrogen relationship in wild plants. In: Givnish T (ed) On the economy of form and function. Cambridge University Press, Cambridge, pp 25–55
Gentscheff G, Gustafsson Å (1940) The balance system of meiosis in Hieracium. Hereditas 26:209–249. https://doi.org/10.1111/j.1601-5223.1940.tb03233.x
Hao GY, Lucero ME, Sanderson SC, Zacharias EH, Holbrook NM (2013) Polyploidy enhances the occupation of heterogeneous environments through hydraulic related trade-offs in Atriplex canescens (Chenopodiaceae). New Phytol 197:970–978. https://doi.org/10.1111/nph.12051
Hartmann M, Štefánek M, Zdvořák P, Heřman P, Chrtek jun J, Mráz P (2017) The Red Queen hypothesis and geographical parthenogenesis in the alpine hawkweed Hieracium alpinum (Asteraceae). Biol J Linn Soc 122:681–696. https://doi.org/10.1093/biolinnean/blx105
Hewitt GM (1999) Post-glacial re-colonization of European biota. Biol J Linn Soc 68:87–112. https://doi.org/10.1111/j.1095-8312.1999.tb01160.x
Hobbie EA, Macko SA, Shugart HH (1999) Insights into nitrogen and carbon dynamics of ectomycorrhizal and saprotrophic fungi from isotopic evidence. Oecologia 118:353–360. https://doi.org/10.1007/s004420050736
Hobbie SE, Schimel JP, Trumbore SE, Randerson JR (2000) Controls over carbon storage and turnover in high-latitude soils. Glob Change Biol 6:196–210. https://doi.org/10.1046/j.1365-2486.2000.06021.x
Hörandl E (2006) The complex causality of geographical parthenogenesis. New Phytol 171:525–538. https://doi.org/10.1111/j.1469-8137.2006.01769.x
Hull-Sanders HM, Johnson RH, Owen HA, Meyer GA (2009) Effects of polyploidy on secondary chemistry, physiology, and performance of native and invasive genotypes of Solidago gigantea (Asteraceae). Am J Bot 96:762–770. https://doi.org/10.3732/ajb.1500995
Inauen N, Körner C, Hiltbrunner E (2012) No growth stimulation by CO2 enrichment in alpine glacier forefield plants. Glob Change Biol 18:985–999. https://doi.org/10.1111/j.1365-2486.2011.02584.x
Iqbal M (1983) An introduction to solar radiation, 1 edn. Academic Press, London
Körner C, Farquhar G, Wong S (1991) Carbon isotope discrimination by plants follows latitudinal and altitudinal trends. Oecologia 88:30–40. https://doi.org/10.1007/BF00328400
Körner C, Diemer M, Schäppi B, Zimmermann L (1996) Response of alpine vegetation to elevated CO2. In: Koch GW, Roy J (eds) Carbon dioxide and terrestrial ecosystems. Academic Press, San Diego, pp 177–196
Körner C, Leuzinger S, Riedl S, Siegwolf RT, Streule L (2016) Carbon and nitrogen stable isotope signals for an entire alpine flora, based on herbarium samples. Alp Bot 126:153–166. https://doi.org/10.1007/s00035-016-0170-x
Laureano RG, Lazo YO, Linares JC, Luque A, Martínez F, Seco JI, Merino J (2008) The cost of stress resistance: construction and maintenance costs of leaves and roots in two populations of Quercus ilex. Tree Physiol 28:1721–1728. https://doi.org/10.1093/treephys/28.11.1721
Leitch A, Leitch I (2008) Genomic plasticity and the diversity of polyploid plants. Science 320:481–483. https://doi.org/10.1126/science.1153585
Levin DA (2002) The role of chromosomal change in plant evolution. Oxford University Press, New York
Lewis WM Jr (1985) Nutrient scarcity as an evolutionary cause of haploidy. Am Nat 125:692–701. https://doi.org/10.1086/284372
Lloyd J, Taylor J (1994) On the temperature dependence of soil respiration. Funct Ecol 8:315–323. https://doi.org/10.2307/2389824
Maherali H, Walden AE, Husband BC (2009) Genome duplication and the evolution of physiological responses to water stress. New Phytol 184:721–731. https://doi.org/10.1111/j.1469-8137.2009.02997.x
Manzaneda AJ, Rey PJ, Bastida JM, Weiss-Lehman C, Raskin E, Mitchell-Olds T (2012) Environmental aridity is associated with cytotype segregation and polyploidy occurrence in Brachypodium distachyon (Poaceae). New Phytol 193:797–805. https://doi.org/10.1111/j.1469-8137.2011.03988.x
Maron JL, Elmendorf SC, Vilà M (2007) Contrasting plant physiological adaptation to climate in the native and introduced range of Hypericum perforatum. Evolution 61:1912–1924. https://doi.org/10.1111/j.1558-5646.2007.00153.x
Marron N, Dreyer E, Boudouresque E, Delay D, Petit J-M, Delmotte FM, Brignolas F (2003) Impact of successive drought and re-watering cycles on growth and specific leaf area of two Populus × canadensis (Moench) clones, ‘Dorskamp’ and ‘Luisa_Avanzo’. Tree Physiol 23:1225–1235. https://doi.org/10.1093/treephys/23.18.1225
Mattson WJ Jr (1980) Herbivory in relation to plant nitrogen content. Annu Rev Ecol Syst 11:119–161. https://doi.org/10.1146/annurev.es.11.110180.001003
Michelsen A, Schmidt IK, Jonasson S, Quarmby C, Sleep D (1996) Leaf 15N abundance of subarctic plants provides field evidence that ericoid, ectomycorrhizal and non-and arbuscular mycorrhizal species access different sources of soil nitrogen. Oecologia 105:53–63. https://doi.org/10.1007/BF00328791
Mráz P (2003) Mentor effects in the genus Hieracium s. str. (Compositae, Lactuceae). Folia Geobot 38:345–350. https://doi.org/10.1007/BF02803204
Mráz P, Chrtek J, Šingliarová B (2009) Geographical parthenogenesis, genome size variation and pollen production in the arctic-alpine species Hieracium alpinum. Bot Helv 119:41–51. https://doi.org/10.1007/s00035-009-0055-3
Mráz P, Bourchier RS, Treier UA, Schaffner U, Müller-Schärer H (2011) Polyploidy in phenotypic space and invasion context: a morphometric study of Centaurea stoebe sl. Int J Plant Sci 172:386–402. https://doi.org/10.1086/658151
Mustard MJ, Standing DB, Aitkenhead MJ, Robinson D, McDonald AJS (2003) The emergence of primary strategies in evolving virtual-plant populations. Evol Ecol Res 5:1067–1081
Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara R, Simpson GL, Solymos P, Stevens MHH, Wagner H (2015) vegan: community ecology package. R package version 2.4-5. R Foundation for Statistical Computing, Vienna
Parisod C, Holderegger R, Brochmann C (2010) Evolutionary consequences of autopolyploidy. New Phytol 186:5–17. https://doi.org/10.1111/j.1469-8137.2009.03142.x
Pinheiro J, Bates D, DebRoy S, Sarkar D, Team RC (2017) nlme: linear and nonlinear mixed effects models. R package version 3.1–131. R Foundation for Statistical Computing, Vienna
Poorter H, van de Vijver CA, Boot RG, Lambers H (1995) Growth and carbon economy of a fast-growing and a slow-growing grass species as dependent on nitrate supply. Plant Soil 171:217–227. https://doi.org/10.1007/BF00010275
Poorter H, Berkel Yv, Baxter R, Hertog Jd, Dijkstra P, Gifford R, Griffin K, Roumet C, Roy J, Wong S (1997) The effect of elevated CO2 on the chemical composition and construction costs of leaves of 27 C3 species. Plant Cell Environ 20:472–482. https://doi.org/10.1046/j.1365-3040.1997.d01-84.x
R Core Team (2014) R: a language and environment for statistical computing. Version 3.1.2. R Foundation for Statistical Computing, Vienna
Ramsey J, Schemske DW (1998) Pathways, mechanisms, and rates of polyploid formation in flowering plants. Annu Rev Ecol Syst 29:467–501. https://doi.org/10.1146/annurev.ecolsys.29.1.467
Reekie E, Bazzaz F (1987) Reproductive effort in plants. 2. Does carbon reflect the allocation of other resources? Am Nat 129:897–906. https://doi.org/10.1086/284682
Reich PB, Oleksyn J (2004) Global patterns of plant leaf N and P in relation to temperature and latitude. Proc Natl Acad Sci USA 101:11001–11006. https://doi.org/10.1073/pnas.0403588101
Reich PB, Walters MB, Ellsworth DS (1997) From tropics to tundra: global convergence in plant functioning. Proc Natl Acad Sci USA 94:13730–13734
Reich PB, Ellsworth DS, Walters MB, Vose JM, Gresham C, Volin JC, Bowman WD (1999) Generality of leaf trait relationships: a test across six biomes. Ecology 80:1955–1969. https://doi.org/10.1890/0012-9658(1999)080%5B1955:GOLTRA%5D2.0.CO;2
Rosenberg O (1927) Die semiheterotypische Teilung und ihre Bedeutung für die Entstehung verdoppelter Chromosomenzahlen. Hereditas 8:305–338. https://doi.org/10.1111/j.1601-5223.1927.tb03165.x
Scheepens J, Frei ES, Stöcklin J (2010) Genotypic and environmental variation in specific leaf area in a widespread alpine plant after transplantation to different altitudes. Oecologia 164:141–150. https://doi.org/10.1007/s00442-010-1650-0
Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675. https://doi.org/10.1038/nmeth.2089
Shaver G, Chapin F III, Gartner BL (1986) Factors limiting seasonal growth and peak biomass accumulation in Eriophorum vaginatum in Alaskan tussock tundra. J Ecol. https://doi.org/10.2307/2260362
Sinclair T (1975) Photosynthate and nitrogen requirements for seed production by various crops. Science 189:565–567. https://doi.org/10.1126/science.189.4202.565
Sitch S et al (2003) Evaluation of ecosystem dynamics, plant geography and terrestrial carbon cycling in the LPJ dynamic global vegetation model. Glob Change Biol 9:161–185. https://doi.org/10.1046/j.1365-2486.2003.00569.x
Soltis DE, Soltis PS, Schemske DW, Hancock JF, Thompson JN, Husband BC, Judd WS (2007) Autopolyploidy in angiosperms: have we grossly underestimated the number of species? Taxon 56:13–30. https://doi.org/10.2307/25065732
Sterner RW, Elser JJ (2002) Ecological stoichiometry: the biology of elements from molecules to the biosphere. Princeton University Press, Princeton
Thébault A, Gillet F, Müller-Schärer H, Buttler A (2011) Polyploidy and invasion success: trait trade-offs in native and introduced cytotypes of two Asteraceae species. Plant Ecol 212:315–325. https://doi.org/10.1007/s11258-010-9824-8
Thompson KA, Husband BC, Maherali H (2014) Climatic niche differences between diploid and tetraploid cytotypes of Chamerion angustifolium (Onagraceae). Am J Bot 101:1868–1875. https://doi.org/10.3732/ajb.1400184
Vandel APM (1928) La parthénogenese géographique. Contribution à l’étude biologique et cytologique de la parthénogenese naturelle. Bulletin Biologique de la France et de la Belgique 62:164–182
Vile D, Garnier E, Shipley B, Laurent G, Navas M-L, Roumet C, Lavorel S, Diaz S, Hodgson JG, Lloret F (2005) Specific leaf area and dry matter content estimate thickness in laminar leaves. Ann Bot 96:1129–1136. https://doi.org/10.1093/aob/mci264
Welker JM, Jónsdóttir IS, Fahnestock JT (2003) Leaf isotopic (δ13C and δ15N) and nitrogen contents of Carex plants along the Eurasian Coastal Arctic: results from the Northeast Passage expedition. Polar Biol 27:29–37. https://doi.org/10.1007/s00300-003-0562-4
Wellstein C, Poschlod P, Gohlke A, Chelli S, Campetella G, Rosbakh S, Canullo R, Kreyling J, Jentsch A, Beierkuhnlein C (2017) Effects of extreme drought on specific leaf area of grassland species: a meta-analysis of experimental studies in temperate and sub-Mediterranean systems. Glob Change Biol 23:2473–2481. https://doi.org/10.1111/gcb.13662
Wright IJ, Westoby M (2002) Leaves at low versus high rainfall: coordination of structure, lifespan and physiology. New Phytol 155:403–416. https://doi.org/10.1046/j.1469-8137.2002.00479.x
Zhu Y, Siegwolf RT, Durka W, Körner C (2010) Phylogenetically balanced evidence for structural and carbon isotope responses in plants along elevational gradients. Oecologia 162:853–863. https://doi.org/10.1007/s00442-009-1515-6
Acknowledgements
We thank V. Mrázová and L. Vondrovicová for their help with the preparation of samples for IRMS analyses and L. Vlk for the measurements of the SLA. The work was financially supported by the Czech Science Foundation (GAČR Grant no. 14-02858S). The IRMS equipment used for this study was purchased from the Operational Programme Prague-Competitiveness (Project CZ.2.16/3.1.00/21516). Institutional Funding for K. J. was provided by the Center for Geosphere Dynamics (UNCE/SCI/006); for J. C. by a long-term research development Project no. RVO 67985939 of the Czech Academy of Sciences.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
35_2018_210_MOESM2_ESM.tiff
Fig S1: Association between specific leaf area (SLA) and foliar N content of diploid (2x) and triploid (3x) plants of Hieracium alpinum and Scandinavian triploid (SCV 3x) and continental European triploid (CEU 3x) plants. Ablines represent the correlation between tested variables, independently for each of the two groups per plot (dashed) and across all individuals depict per plot (solid) (TIFF 192 KB)
35_2018_210_MOESM3_ESM.png
Fig S2 Results of the variance partitioning analyses. Proportions of explained variation of eco-physiological leaf traits of diploid and triploid Hieracium alpinum plants by the cytotype and the abiotic factors and their interactions. Tested fixed effects: mean temperature during growing season (May – September; TDUGS); amount of precipitation during the growing season (May–September; PDUGS); amount of solar radiation during the growing season (May–September; SDUGS); populations’ elevational position (ELEV; solely for δ13C). Values < 0.0005 are not shown (PNG 566 KB)
35_2018_210_MOESM4_ESM.png
Fig S3 Results of the variance partitioning analyses. Proportion of explained variation of eco-physiological leaf traits of diploid and triploid Hieracium alpinum plants by the cytotype and the biotic factors and their interactions. Tested fixed effects: number of co-occurring vascular plant species (Richness); cover by herb and shrub layer (E1 cover); cover by bryophyte and lichens layer (E0 cover). Values < 0.0005 are not shown (PNG 511 KB)
35_2018_210_MOESM5_ESM.png
Fig S4 Latitudinal gradients in eco-physiological leaf traits of diploid (2x) and triploid populations of Hieracium alpinum. Size of the data points corresponds to level of referring population mean. Foliar carbon content; Foliar carbon-to-nitrogen ratio (C/N ratio); Specific leaf area (SLA); Foliar δ15N; Foliar N content; Foliar δ13C (PNG 1213 KB)
35_2018_210_MOESM6_ESM.png
Fig S5: Boxplots of eco-physiological leaf traits in diploid and triploid populations of Hieracium alpinum sorted by latitudinal position. One boxplot represents one population; dashed lines represent average across all populations of the diploid, continental triploid, and Scandinavian triploid range, respectively. Specific leaf area (SLA); foliar nitrogen content; foliar carbon content; foliar carbon-to-nitrogen ratio; foliar δ 13C; foliar δ15N (PNG 972 KB)
35_2018_210_MOESM7_ESM.tiff
Fig S6. Boxplots of local abiotic environment in diploid (2x) and triploid (3x) populations of Hieracium alpinum and Scandinavian triploid (SCV 3x) and continental European triploid (CEU 3x) populations. Abiotic environment abbreviations: TDUGS—Mean temperature during growing season (May–September); PDUGS—Amount of precipitation during growing season (May–September); SDUGS—amount of solar radiation during the growing season (May–September). Triangles indicate mean values. Only statistically significant differences are displayed ** P < 0.01; *** P < 0.001 (TIFF 199 KB)
35_2018_210_MOESM8_ESM.tiff
Fig S7. Associations between eco-physiological leaf traits of diploid (2x), central European triploid (CEU 3x), and Scandinavian triploid (SCV 3x) populations of Hieracium alpinum and traits important for dispersal (height of inflorescence; a, b) and reproduction (capitulum size; c, d), both assessed at the level of individual plants. Overall associations are indicated by dashed lines. Foliar nitrogen content (foliar N [%]); foliar δ15N [‰] (TIFF 343 KB)
35_2018_210_MOESM9_ESM.tif
Fig S8. Hieracium alpinum plants of the same age in outdoor pots (growing in the same soil) in the botanical garden of Průhonice, the Czech Republic. The offspring of Scandinavian plants in the front is significantly smaller compared to offspring of other plants in the back, irrespective of the cytotype (TIF 3739 KB)
Rights and permissions
About this article
Cite this article
Hartmann, M., Jandová, K., Chrtek, J. et al. Effects of latitudinal and elevational gradients exceed the effects of between-cytotype differences in eco-physiological leaf traits in diploid and triploid Hieracium alpinum. Alp Botany 128, 133–147 (2018). https://doi.org/10.1007/s00035-018-0210-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00035-018-0210-9