Skip to main content

Advertisement

Log in

Marginal Calluna populations are more resistant to climate change, but not under high-nitrogen loads

  • Published:
Plant Ecology Aims and scope Submit manuscript

Abstract

The dominant plant species of European heathlands Calluna vulgaris is considered vulnerable to drought and enhanced nitrogen (N) loads. However, impacts may vary across the distribution range of Calluna heathlands. We tested the hypothesis that Calluna of southern and eastern marginal populations (MP) are more resistant to drought events than plants of central populations (CP), and that this is mainly due to trait differences such as biomass allocation patterns. Furthermore, we hypothesised that N fertilisation can offset differences in drought susceptibility between CP and MP. We conducted a full-factorial 2-year greenhouse experiment with Calluna plants of CP and MP and quantified growth responses in terms of biomass production, allocation and tissue δ13C signatures. Biomass production, shoot–root ratios and tissue δ13C values of 1-year-old plants were higher for CP than for MP, indicating a higher drought susceptibility of CP. These trait differences were not observed for 2-year-old plants. N fertilisation increased shoot–root ratios of 1- and 2-year-old plants and across populations due to a stimulation of the aboveground biomass allocation. As a consequence, population-related differences in drought susceptibility were offset for N-fertilised plants. We concluded that Calluna plants originating from different populations developed adaptive traits to local climates, which determined their drought sensitivity. However, the higher drought resistance of MP can be attenuated by an N-induced increase in shoot–root ratios. This suggests that analyses on plant growth responses to global change should include multi-factor approaches with a focus on different populations throughout a species’ distribution range.

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

Similar content being viewed by others

References

  • Albert KR, Mikkelsen TN, Michelsen A, Ro-Poulsen H, van der Linden L (2011) Interactive effects of drought, elevated CO2 and warming on photosynthetic capacity and photosystem performance in temperate heath plants. J Plant Physiol 168:1550–1561

    Article  PubMed  CAS  Google Scholar 

  • Alonso I, Hartley SE (1998) Effects of nutrient supply, light availability and herbivory on the growth of heather and three competing grass species. Plant Ecol 137:203–212

    Article  Google Scholar 

  • Andresen LC, Michelsen A, Jonasson S, Schmidt IK, Mikkelsen TN, Ambus P, Beier C (2010) Plant nutrient mobilization in temperate heathland responds to elevated CO2, temperature and drought. Plant Soil 328:381–396

    Article  CAS  Google Scholar 

  • Aranda I, Alía R, Ortega U, Dantas ÂK, Majada J (2010) Intra-specific variability in biomass partitioning and carbon isotopic discrimination under moderate drought stress in seedlings from four Pinus pinaster populations. Tree Genet Genomes 6:169–178

    Article  Google Scholar 

  • Arndal MF, Merrild MP, Michelsen A, Schmidt IK, Mikkelsen TN, Beier C (2013) Net root growth and nutrient acquisition in response to predicted climate change in two contrasting heathland species. Plant Soil 369:615–629

    Article  CAS  Google Scholar 

  • Aspelmeier S, Leuschner C (2004) Genotypic variation in drought response of silver birch (Betula pendula): leaf water status and carbon gain. Tree Physiol 24:517–528

    Article  PubMed  CAS  Google Scholar 

  • Bates DM, Maechler M, Bolker B, Walker S (2014) lme4: Linear mixed-effects models using Eigen and S4. R package version 1.1-6. Available at http://CRAN.R-project.org/package=lme4

  • Bobbink R, Hicks K, Galloway J, Spranger T, Alkemade R, Ashmore M, Bustamante M, Cinderby S, Davidson E, Dentener F, Emmett B, Erisman J-W, Fenn M, Gilliam F, Nordin A, Pardo L, de Vries W (2010) Global assessment of nitrogen deposition effects on terrestrial plant diversity: a synthesis. Ecol Appl 20:30–59

    Article  PubMed  CAS  Google Scholar 

  • Borchard F, Buchholz S, Helbing F, Fartmann T (2014) Carabid beetles and spiders as bioindicators for the evaluation of montane heathland restoration on former spruce forests. Biol Conserv 178:185–192

    Article  Google Scholar 

  • Bretz F, Hothorn T, Westfall P (2010) Multiple comparisons using R. CRC Press, Boca Raton

    Book  Google Scholar 

  • Chaves MM, Pereira JS, Maroco J, Rodrigues ML, Ricardo CPP, Osório ML, Carvalho I, Faria T, Pinheiro C (2002) How plants cope with water stress in the field. Photosynthesis and growth. Ann Bot 89:907–916

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Crawley MJ (2007) The R book. Wiley, Chichester

    Book  Google Scholar 

  • Farquhar GD, O’Leary MH, Berry JA (1982) On the relationship between carbon isotope discrimination and the intercellular carbon dioxide concentration in leaves. Aust J Plant Physiol 9:121–137

    Article  CAS  Google Scholar 

  • Farquhar GD, Ehleringer JR, Hubick KT (1989) Carbon isotope discrimination and photosynthesis. Annu Rev Plant Physiol Plant Mol Biol 40:503–537

    Article  CAS  Google Scholar 

  • Friedrich U, von Oheimb G, Kriebitzsch W-U, Schleßelmann K, Weber MS, Härdtle W (2012) Nitrogen deposition increases susceptibility to drought - experimental evidence with the perennial grass Molinia caerulea (L.) Moench. Plant Soil 353:59–71

    Article  CAS  Google Scholar 

  • Gieger T, Thomas FM (2002) Effects of defoliation and drought stress on biomass partitioning and water relations of Quercus robur and Quercus petraea. Basic Appl Ecol 3:171–181

    Article  Google Scholar 

  • Gimingham CH (1972) Ecology of heathlands. London Chapman Hall, London

    Google Scholar 

  • Gordon C, Woodin SJ, Alexander IJ, Mullins CE (1999a) Effects of increased temperature, drought and nitrogen supply on two upland perennials of contrasting functional type: Calluna vulgaris and Pteridium aquilinum. New Phytol 142:243–258

    Article  Google Scholar 

  • Gordon C, Woodin SJ, Mullins CE, Alexander IJ (1999b) Effects of environmental change, including drought, on water use by competing Calluna vulgaris (heather) and Pteridium aquilinum (bracken). Funct Ecol 13:96–106

    Article  Google Scholar 

  • Gorissen A, Tietema A, Joosten NN, Estiarte M, Peñuelas J, Sowerby A, Emmett BA, Beier C (2004) Climate change affects carbon allocation to the soil in shrublands. Ecosystems 7:650–661

    Article  CAS  Google Scholar 

  • Härdtle W, von Oheimb G, Niemeyer M, Niemyer T, Assmann T, Meyer H (2007) Nutrient leaching in dry heathland ecosystems: effects of atmospheric deposition and management. Biogeochemistry 86:201–205

    Article  Google Scholar 

  • Instituto Tecnológico Geominero de España (1995) Atlas del medio natural de la provincia de León. Diputación de León, León

    Google Scholar 

  • IPCC (2013) Climate change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. IN: Stocker TF, Qin D, Plattner GK, Tignor M, Allen SK, Boschung J, Nauels A, Xia Y, Bex V, Midgley PM (eds) Cambridge University Press, Cambridge and New York, NY

  • Kuster T, Arend M, Günthardt-Goerg M, Schulin R (2013) Root growth of different oak provenances in two soils under drought stress and air warming conditions. Plant Soil 369:61–71

    Article  CAS  Google Scholar 

  • Kuznetsova A, Brockhoff PB, Christensen RHB (2014) lmerTest: Tests for random and fixed effects for linear mixed effect models (lmer objects of lme4 package). R package version 2.0-6. Available at http://CRAN.R-project.org/package=lmerTest

  • Lauteri M, Pliura A, Monteverdi MC, Brugnoli E, Villani F, Eriksson G (2004) Genetic variation in carbon isotope discrimination in six European populations of Castanea sativa Mill. originating from contrasting localities. J Evol Biol 17:1286–1296

    Article  PubMed  CAS  Google Scholar 

  • Loidi J, Biurrun I, Campos JA, García-Mijangos I, Herrera M (2010) A biogeographical analysis of the European Atlantic lowland heathlands. J Veg Sci 21:832–842

    Article  Google Scholar 

  • Macel M, Lawson CS, Mortimer SR, Šmilauerova M, Bischoff A, Crémieux L, Doležal J, Edwards AR, Lanta V, Bezemer TM, van der Putten WH, Igual JM, Rodriguez-Barrueco C, Müller-Schärer H, Steinger T (2007) Climate versus soil factors in local adaptation of two common plant species. Ecology 88:424–433

    Article  PubMed  Google Scholar 

  • Marrs RH (1986) The role of catastrophic death of Calluna in heathland dynamics. Vegetatio 66:109–115

    Google Scholar 

  • Marrs RH, Diemont WH (2013) Succession theory and management of heathlands. In: Diemont WH, Heijmam WJM, Siepel H, Webb NR (eds) The ecology and economy of heathlands. KNNV Publishing, Zeist, pp 187–199

    Google Scholar 

  • McConnaughay KDM, Coleman JS (1999) Biomass allocation in plants: ontogeny or optimality? A test along three resource gradients. Ecology 80:2581–2593

    Article  Google Scholar 

  • Meyer-Grünefeldt M, Calvo L, Marcos E, von Oheimb G, Härdtle W (2015) Impacts of drought and nitrogen addition on Calluna-heathlands differ with plant life-history stage. J Ecol 103:1141–1152

    Article  Google Scholar 

  • Peuke AD, Rennenberg H (2004) Carbon, nitrogen, phosphorus, and sulphur concentration and partitioning in beech ecotypes (Fagus sylvatica L.): phosphorus most affected by drought. Trees-Struct Funct 18:639–648

    Article  CAS  Google Scholar 

  • Phoenix GK, Emmett BA, Britton AJ, Caporn SJM, Dise NB, Helliwell R, Jones L, Leake JR, Leith ID, Sheppard LJ, Sowerby A, Pilkington MG, Rowe EC, Ashmore MR, Power SA (2012) Impacts of atmospheric nitrogen deposition: responses of multiple plant and soil parameters across contrasting ecosystems in long-term field experiments. Global Chang Biol 18:1197–1215

    Article  Google Scholar 

  • Picon C, Guehl JM, Ferhi A (1996) Leaf gas exchange and carbon isotope composition responses to drought in a drought-avoiding (Pinus pinaster) and a drought-tolerant (Quercus petraea) species under present and elevated atmospheric CO2 concentrations. Plant Cell Environ 19:182–190

    Article  Google Scholar 

  • Richter S, Kipfer T, Wohlgemuth T, Calderón Guerrero C, Ghazoul J, Moser B (2012) Phenotypic plasticity facilitates resistance to climate change in a highly variable environment. Oecologia 169:269–279

    Article  PubMed  Google Scholar 

  • Rose L, Leuschner C, Köckemann B, Buschmann H (2009) Are marginal beech (Fagus sylvatica L.) provenances a source for drought tolerant ecotypes? Eur J For Res 128:335–343

    Article  Google Scholar 

  • Sæbø A, Håland Å, Skre O, Mortensen LM (2001) Influence of nitrogen and winter climate stresses on Calluna vulgaris (L.) Hull. Ann Bot 88:823–828

    Article  Google Scholar 

  • Sala OE, Chapin FS III, Armesto JJ, Berlow E, Bloomfield J, Dirzo R, Huber-Sanwald E, Huenneke LF, Jackson RB, Kinzig A, Leemans R, Lodge DM, Mooney HA, Oesterheld M, Poff NL, Sykes MT, Walker BH, Walker M, Wall DH (2000) Global biodiversity scenarios for the year 2100. Science 287:1770–1774

    Article  PubMed  CAS  Google Scholar 

  • Schär C, Vidale PL, Lüthi D, Frei C, Häberli C, Liniger MA, Appenzeller C (2004) The role of increasing temperature variability in European summer heatwaves. Nature 427:332–336

    Article  PubMed  Google Scholar 

  • Southon GE, Green ER, Jones AG, Barker CG, Power SA (2012) Long-term nitrogen additions increase likelihood of climate stress and affect recovery from wildfire in a lowland heath. Global Chang Biol 18:2824–2837

    Article  Google Scholar 

  • Vandvik V, Topper JP, Cook Z, Daws MI, Heegaard E, Maren IE, Velle LG (2014) Management-driven evolution in a domesticated ecosystem. Biol Lett. doi:10.1098/rsbl.2013.1082

    PubMed  Google Scholar 

  • von Oheimb G, Power SA, Falk K, Friedrich U, Mohamed A, Krug A, Boschatzke N, Härdtle W (2010) N:P ratio and the nature of nutrient limitation in Calluna-dominated heathlands. Ecosystems 13:317–327

    Article  CAS  Google Scholar 

  • Weiner J (2004) Allocation, plasticity and allometry in plants. Perspect Plant Ecol Evol Syst 6:207–215

    Article  Google Scholar 

  • Yordanov I, Velikova V, Tsonev T (2000) Plant responses to drought, acclimation, and stress tolerance. Photosynthetica 38:171–186

    Article  CAS  Google Scholar 

  • Zavaleta ES, Shaw MR, Chiariello NR, Mooney HA, Field CB (2003) Additive effects of simulated climate changes, elevated CO2, and nitrogen deposition on grassland diversity. Proc Natl Acad Sci USA 100:7650–7654

    Article  PubMed  CAS  PubMed Central  Google Scholar 

Download references

Acknowledgments

We would like to thank the Verein Naturschutzpark e.V. and the Naturpark Elbufer-Drawehn for collaboration and for permission to collect seeds in the Lüneburger Heide and the Nemitzer Heide. We are grateful to Susanne Osterloh from the Anhalt University of Applied Sciences for collecting seeds in the Oranienbaumer Heide. This study was funded by the German Federal Ministry of Education and Research (research project ‘KLIMZUG-NORD’).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Werner Härdtle.

Additional information

Communicated by Miguel Franco.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Meyer-Grünefeldt, M., Belz, K., Calvo, L. et al. Marginal Calluna populations are more resistant to climate change, but not under high-nitrogen loads. Plant Ecol 217, 111–122 (2016). https://doi.org/10.1007/s11258-015-0563-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11258-015-0563-8

Keywords

Navigation