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Legacy effects of land-use modulate tree growth responses to climate extremes

Abstract

Climate change can impact forest ecosystem processes via individual tree and community responses. While the importance of land-use legacies in modulating these processes have been increasingly recognised, evidence of former land-use mediated climate-growth relationships remain rare. We analysed how differences in former land-use (i.e. forest continuity) affect the growth response of European beech to climate extremes. Here, using dendrochronological and fine root data, we show that ancient forests (forests with a long forest continuity) and recent forests (forests afforested on former farmland) clearly differ with regard to climate–growth relationships. We found that sensitivity to climatic extremes was lower for trees growing in ancient forests, as reflected by significantly lower growth reductions during adverse climatic conditions. Fine root morphology also differed significantly between the former land-use types: on average, trees with high specific root length (SRL) and specific root area (SRA) and low root tissue density (RTD) were associated with recent forests, whereas the opposite traits were characteristic of ancient forests. Moreover, we found that trees of ancient forests hold a larger fine root system than trees of recent forests. Our results demonstrate that land-use legacy-mediated modifications in the size and morphology of the fine root system act as a mechanism in regulating drought resistance of beech, emphasising the need to consider the ‘ecological memory’ of forests when assessing or predicting the sensitivity of forest ecosystems to global environmental change.

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References

  1. Allen CD, Macalady AK, Chenchouni H, Bachelet D, McDowell N, Vennetier M, Kitzberger T, Rigling A, Breshears DD, Hogg EHT, Gonzalez P, Fensham R, Zhang Z, Castro J, Demidova N, Lim J-H, Allard G, Running SW, Semerci A, Cobb N (2010) A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests. For Ecol Manag 259:660–684. https://doi.org/10.1016/j.foreco.2009.09.001

    Article  Google Scholar 

  2. Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:31–46. https://doi.org/10.1111/j.1442-9993.2001.01070.pp.x

    Article  Google Scholar 

  3. Aranda I, Gil-Pelegrín E, Gascó A, Guevara MA, Cano JF, De Miguel M, Ramírez-Valiente JA, Peguero-Pina JJ, Perdiguero P, Soto A, Cervera MT, Collada C (2012) Drought response in forest trees: from the species to the gene. In: Aroca R (ed) Plant responses to drought stress. Springer, Berlin, Heidelberg, pp 293–333. https://doi.org/10.1007/978-3-642-32653-0_12

    Chapter  Google Scholar 

  4. Bardgett RD, Mommer L, De Vries FT (2014) Going underground: root traits as drivers of ecosystem processes. Trends Ecol Evol 29:692–699. https://doi.org/10.1016/j.tree.2014.10.006

    Article  PubMed  Google Scholar 

  5. Bellassen V, Luyssaert S (2014) Managing forests in uncertain times. Nature 506:153–155

    Article  PubMed  Google Scholar 

  6. Bradford MA, Wood SA, Maestre FT, Reynolds JF, Warren RJ II (2012) Contingency in ecosystem but not plant community response to multiple global change factors. New Phytol 196:462–471. https://doi.org/10.1111/j.1469-8137.2012.04271.x

    Article  PubMed  Google Scholar 

  7. Brunner I, Herzog C, Dawes MA, Arend M, Sperisen C (2015) How tree roots respond to drought. Front Plant Sci 6:547. https://doi.org/10.3389/fpls.2015.00547

    Article  PubMed  PubMed Central  Google Scholar 

  8. Buckley DH, Schmidt TM (2001) The structure of microbial communities in soil and the lasting impact of cultivation. Microb Ecol 42:11–21. https://doi.org/10.1007/s002480000108

    PubMed  CAS  Article  Google Scholar 

  9. Buyan U, Zang C, Menzel A (2017) Different responses of multispecies tree ring growth to various drought indices across Europe. Dendrochronologia 44:1–8. https://doi.org/10.1016/j.dendro.2017.02.002

    Article  Google Scholar 

  10. Cavin L, Jump AS (2016) Highest drought sensitivity and lowest resistance to growth suppression are found in the range core of the tree Fagus sylvatica L. not the equatorial range edge. Glob Change Biol 23:362–379. https://doi.org/10.1111/gcb.13366

    Article  Google Scholar 

  11. Chambers JQ, Higuchi N, Tribuzy ES, Trumbore SE (2001) Carbon sink for a century. Nature 410:429. https://doi.org/10.1038/35068624

    Article  PubMed  CAS  Google Scholar 

  12. Comas LH, Callahan HS, Midford P (2014) Patterns in root traits of woody species hosting arbuscular and ectomycrrhizas: implications for the evolution of belowground strategies. Ecol Evol 4:2979–2990. https://doi.org/10.1002/ece3.1147

    Article  PubMed  PubMed Central  Google Scholar 

  13. Compton JA, Boone RD (2000) Long-term impacts of agriculture on soil carbon and nitrogen in New England forests. Ecology 81:2314–2330. https://doi.org/10.1890/0012-9658(2000)081[2314:LTIOAO]2.0.CO;2

    Article  Google Scholar 

  14. Dammann I, Paar U, Weymar J, Spielmann M, Eichhorn J (2016) Waldzustandsbericht 2016 für Schleswig-Holstein. Printec Offset Kassel, Germany

    Google Scholar 

  15. De la Peña E, Baeten L, Steel H, Viaene N, De Sutter N, De Schrijver A, Verheyen K (2016) Beyond plant-soil feedbacks: mechanisms driving plant community shifts due to land-use legacies in post-agricultural forests. Funct Ecol 30:1073–1085. https://doi.org/10.1111/1365-2435.12672

    Article  Google Scholar 

  16. De Martonne E (1926) Aréisme et indice d’aridité. C R Acad Sci 181:1395–1398

    Google Scholar 

  17. Di Filippo A, Biondi F, Cufar K, De Luis M, Grabner M, Maugeri M, Saba EP, Schirone B, Piovesan G (2007) Bioclimatology of beech (Fagus sylvatica L.) in the Eastern Alps: spatial and altitudinal climatic signals identifies through a tree-ring network. J Biogeogr 34:1873–1892. https://doi.org/10.1111/j.1365-2699.2007.01747.x

    Article  Google Scholar 

  18. Drobyshev I, Övergaard R, Saygin I, Niklasson M, Hickler T, Karlsson M, Sykes MT (2010) Masting behaviour and dendrochronology of European beech (Fagus sylvatica L.) in southern Sweden. For Ecol Manag 259:2160–2171. https://doi.org/10.1016/j.foreco.2010.01.037

    Article  Google Scholar 

  19. Dulamsuren C, Hauck M, Kopp G, Ruff M, Leuschner C (2017) European beech responds to climate change with growth decline at lower, and growth increase at higher elevations in the center of its distribution range (SW Germany). Trees 31:673–686. https://doi.org/10.1007/s00468-016-1499-x

    Article  Google Scholar 

  20. DWD Climate Data Center (CDC) (2017) Historical monthly station observations (temperature, pressure, precipitation, sunshine duration, etc.) for Germany, version v005

  21. Dziedek C, Härdtle W, von Oheimb G, Fichtner A (2016) Nitrogen addition enhances drought sensitivity of young deciduous tree species. Front Plant Sci 7:1100

    Article  PubMed  PubMed Central  Google Scholar 

  22. Dziedek C, Fichtner A, Calvo L, Marcos E, Jansen K, Kunz M, Walmsley D, von Oheimb G, Härdtle W (2017) Phenotypic plasticity explains response patterns of European beech (Fagus sylvatica L.) saplings to nitrogen fertilization and drought events. Forests 8(91):1–11. https://doi.org/10.3390/f8030091

    Article  Google Scholar 

  23. Eissenstat DM, Yanai RD (1997) The ecology of root lifespan. Adv Ecol Res 27:1–60. https://doi.org/10.1016/S0065-2504(08)60005-7

    Article  Google Scholar 

  24. Eissenstat DM, Wells CE, Yanai RD, Whitbeck JL (2000) Building roots in a changing environment: implications for root longevity. New Phytol 147:33–42

    Article  CAS  Google Scholar 

  25. Fichtner A, von Oheimb G, Härdtle W, Wilken C, Gutknecht JLM (2014) Effects of anthropogenic disturbances on soil microbial communities in oak forests persist for more than 100 years. Soil Biol Biochem 70:79–87. https://doi.org/10.1016/j.soilbio.2013.12.015

    Article  CAS  Google Scholar 

  26. Flinn KM, Vellend M (2005) Recovery of forest plant communities in post-agricultural landscapes. Front Ecol Environ 3:243–250. https://doi.org/10.1890/1540-9295(2005)003[0243:ROFPCI]2.0.CO;2

    Article  Google Scholar 

  27. Foster D, Swanson F, Aber J, Burke I, Brokaw N, Tilman D, Knapp A (2003) The importance of land-use legacies to ecology and conservation. Bioscience 53:77–88. https://doi.org/10.1641/0006-3568(2003)053[0077:TIOLUL]2.0.CO;2

    Article  Google Scholar 

  28. Fraterrigo JM (2013) Landscape legacies. In: Levin SA (ed) Encyclopedia of biodiversity. Academic Press, Waltham, pp 524–530

    Chapter  Google Scholar 

  29. Fraterrigo JM, Balser TC, Turner MG (2006) Microbial community variation and its relationship with nitrogen mineralization in historically altered forests. Ecology 87:570–579. https://doi.org/10.1890/05-0638

    Article  PubMed  Google Scholar 

  30. Freschet GT, Valverde-Barrantes OJ, Tucker CM, Craine JM, McCormack L, Violle C, Fort F, Blackwood CB, Urban-Mead KR, Iversen CM, Bonis A, Comas LH, Cornelissen HC, Dong M, Guo D, Hobbie SE, Holdaway RJ, Kembel SW, Makita N, Onipchenko VG, Picon-Cochard C, Reich PB, De la Riva EG, Smith SW, Soudzilovskaia NA, Tjoelker MG, Wardle DA, Roumet C (2017) Climate, soil and plant functional types as drivers of global fine-root trait variation. J Ecol 105:1182–1196. https://doi.org/10.1111/1365-2745.12769

    Article  Google Scholar 

  31. Genet H, Breda N, Dufrene E (2010) Age-related variation in carbon allocation at tree and stand scales in beech (Fagus sylvatica L.) and sessile oak (Quercus petraea (Matt.) Liebl.) using a chronosequence approach. Tree Physiol 30:177–192. https://doi.org/10.1093/treephys/tpp105

    Article  PubMed  CAS  Google Scholar 

  32. Grace JB, Anderson TM, Oleff H, Scheiner SM (2010) On the specification of structural equation models for ecological systems. Ecol Monogr 80:67–87. https://doi.org/10.1890/09-0464.1

    Article  Google Scholar 

  33. Hacket-Pain AJ, Friend AD, Lageard JA, Thomas PA (2015) The influence of masting phenomenon on growth–climate relationships in trees: explaining the influence of previous summers’ climate on ring width. Tree Physiol 35:319–330. https://doi.org/10.1093/treephys/tpv007

    Article  PubMed  Google Scholar 

  34. Hacket-Pain AJ, Cavin L, Friend AD, Jump S (2016) Consistent limitation of growth by high temperature and low precipitation from range core to southern edge of European beech indicates widespread vulnerability to changing climate. Eur J For Res 135:897–909. https://doi.org/10.1007/s10342-016-0982-7

    Article  Google Scholar 

  35. Härdtle W, Niemeyer T, Assmann T, Baiboks S, Fichtner A, Friedrich U, Lang AC, Neuwirth B, Pfister L, Ries C, Schuldt A, Simon N, von Oheimb G (2013) Long-term trends in tree-ring width hand isotope signatures (δ13C, δ15N) of Fagus sylvatica L. on soils with contrasting water supply. Ecosystems 16:1413–1428. https://doi.org/10.1007/s10021-013-9692-x

    Article  CAS  Google Scholar 

  36. Hertel D, Strecker T, Müller-Haubold H, Leuschner C (2013) Fine root biomass and dynamics in beech forests across a precipitation gradient—is optimal resource partitioning theory applicable to water-limited mature trees? J Ecol 101:1183–1200. https://doi.org/10.1111/1365-2745.12124

    Article  Google Scholar 

  37. Hess C, Niemeyer T, Fichtner A, Jansen K, Kunz M, Maneke M, von Wehrden H, Quante M, Walmsley D, von Oheimb G, Härdtle W (2018) Anthropogenic nitrogen deposition alters growth responses of European beech (Fagus sylvatica L.) to climate change. Environ Pollut 233:92–98. https://doi.org/10.1016/j.envpol.2017.10.024

    Article  PubMed  CAS  Google Scholar 

  38. Hoffmann G (1997) VDLUFA Methodenbuch Band I: Die Untersuchung von Böden, 4th edn. VdLUFA, Darmstadt

    Google Scholar 

  39. Holmes RL (1983) Computer-assisted quality control in tree-ring dating and measurement. Tree Ring Bull 43:69–78

    Google Scholar 

  40. IPCC (2013) Summary for policymakers. In Stocker TF et al. (eds) Climate change 2013: the physical science basis. Contribution of working group I to the fifth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge, New York

  41. Johnstone JF, Allen CD, Franklin JF, Frelich LE, Harvey BJ, Higuera PE, Mack MC, Meentemeyer RK, Metz MR, Perry GLW, Schoennagel T, Turner MG (2016) Changing disturbance regimes, ecological memory, and forest resilience. Front Ecol Environ 14:369–378. https://doi.org/10.1002/fee.1311

    Article  Google Scholar 

  42. Kline RB (2014) Principles and practice of structural equation modeling. Guilford Press, New York

    Google Scholar 

  43. Knutzen F, Dulamsuren C, Meier IC, Leuschner C (2017) Recent climate warming-related growth decline impairs European Beech in the center of its distribution range. Ecosystems 20(8):1494–1511

    Article  CAS  Google Scholar 

  44. Kramer-Walter KR, Bellingham PJ, Millar TR, Smissen RB, Richardson SJ, Laughlin DC (2016) Root traits are multidimensional: specific root length is independent from root tissue density and the plant economic spectrum. J Ecol 104:1299–1310. https://doi.org/10.1111/1365-2745.12562

    Article  Google Scholar 

  45. Lebourgeois F, Eberlé P, Mérian P, Seynave I (2014) Social status-mediated tree-ring responses to climate of Abies alba and Fagus sylvatica shift in importance with increasing stand basal area. For Ecol Manag 328:209–218. https://doi.org/10.1016/j.foreco.2014.05.038

    Article  Google Scholar 

  46. Leuschner C, Ellenberg H (2017) Ecology of Central European forests: vegetation ecology of Central Europe, vol I. Springer, Switzerland

    Book  Google Scholar 

  47. Leuschner C, Backes K, Hertel D, Schipka F, Schmitt U, Terborg O, Runge M (2001) Drought responses at leaf, stem and fine root levels of competitive Fagus sylvatica L. and Quercus petraea (Matt.) Liebl. Trees in dry and wet years. For Ecol Manag 149:33–46

    Article  Google Scholar 

  48. Leuschner C, Hertel D, Schmid I, Koch O, Muhs A, Hölscher D (2004) Stand fine root biomass and fine root morphology in old-growth beech forests as a function of precipitation and soil fertility. Plant Soil 258:43–56. https://doi.org/10.1023/B:PLSO.0000016508.20173.80

    Article  CAS  Google Scholar 

  49. Leuschner C, Wulf M, Bäuchler P, Hertel D (2014) Forest continuity as a key determinant of soil carbon and nutrient storage in beech forests on sandy soils in Northern Germany. Ecosystems 17:497–511. https://doi.org/10.1007/s10021-013-9738-0

    Article  CAS  Google Scholar 

  50. McCormack ML, Adams TS, Smithwick EAH, Eissenstat DM (2012) Predicting fine root lifespan from plant functional traits in temperate trees. New Phytol 195:823–831. https://doi.org/10.1111/j.1469-8137.2012.04198.x

    Article  Google Scholar 

  51. Meier IC, Knutzen F, Eder LM, Müller-Haubold H, Göbel M, Bachmann J, Hertel D, Leuschner C (2017) The deep root system of Fagus sylvatica on sandy soil: structure and variation across a precipitation gradient. Ecosystems. https://doi.org/10.1007/s10021-017-0148-6

    Article  Google Scholar 

  52. Metz J, Annighöfer P, Schall P, Zimmermann J, Kahl T, Schulze E-D, Ammer C (2016) Site-adapted admixed tree species reduce drought susceptibility of mature European beech. Glob Change Biol 22:903–920. https://doi.org/10.1111/gcb.13113

    Article  Google Scholar 

  53. 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. https://doi.org/10.1111/1365-2745.12446

    Article  CAS  Google Scholar 

  54. Millard P, Grelet G-A (2010) Nitrogen storage and remobilization by trees: ecophysiological relevance in a changing world. Tree Physiol 30:1083–1095. https://doi.org/10.1093/treephys/tpq042

    Article  PubMed  CAS  Google Scholar 

  55. Mölder I, Leuschner C (2014) European beech grows better and is less drought sensitive in mixed than in pure stands: tree neighbourhood effects on radial increment. Trees 28:777–792. https://doi.org/10.1007/s00468-014-0991-4

    Article  Google Scholar 

  56. Mommer L, Weemstra M (2012) The role of roots in the resource economics spectrum. New Phytol 195:725–727. https://doi.org/10.1111/j.1469-8137.2012.04247.x

    Article  PubMed  Google Scholar 

  57. Müller A (2007) Jahrringanalytische Untersuchungen zum Informationsgehalt von Holzkohle-Rückständen der historischen Meilerköhlerei. PhD thesis, Albert Ludwigs University of Freiburg, Freiburg, Germany

  58. Müller-Haubold H, Hertel D, Leuschner C (2015) Climatic drivers of mast fruiting in European beech and resulting C and N allocation shifts. Ecosystems 18:1083–1100. https://doi.org/10.1007/s10021-015-9885-6

    Article  CAS  Google Scholar 

  59. Oksanen J, Blanchet FG., Friendly M, Kindt R, Legendre P, McGlinn D, Michin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHM, Szoecs E, Wagner H (2016) vegan: community ecology package. R package, version 2.4-0. https://CRAN.R-project.org/package=vegan

  60. Ostonen I, Helmisaari H-S, Borken W, Tedersoo L, Kukumägi M, Bahram M, Lindroos A-J, Nöjd P, Uri V, Merlä P, Asi E, Löhmus K (2011) Fine root foraging strategies in Norway spruce forests across a European climate gradient. Glob Change Biol 17:3620–3632. https://doi.org/10.1111/j.1365-2486.2011.02501.x

    Article  Google Scholar 

  61. Ozbay G, Khatiwada R, Chintapenta LK, Handy EF, Smith SL (2016) Sustainable farm practice: study of total and soluble phosphorus in a poultry farm equipped with heavy use area protection pads, Dover, Delaware. Prof Agric Work J 4:1–17

    Google Scholar 

  62. Packham JR, Thomas PA, Atkinson MD, Degen T (2012) Biological flora of the British Isles: Fagus sylvatica. J Ecol 100:1557–1608. https://doi.org/10.1111/j.1365-2745.2012.02017.x

    Article  Google Scholar 

  63. Perring MP, De Frenne P, Baeten L, Maes SL, Depauw L, Blondeel H, Carón MM, Verheyen K (2016) Global environmental change effects on ecosystems: the importance of land-use legacies. Glob Change Biol 22:1361–1371. https://doi.org/10.1111/gcb.13146

    Article  Google Scholar 

  64. Pinheiro J, Bates D, DebRoy S, Sarkar D, R Core Team (2016) nlme: linear and nonlinear mixed effects models. R package version 3.1-128. http://CRAN.R-project.org/package=nlme

  65. Reich PB (2014) The world-wide ‘fast–slow’ plant economics spectrum: a traits manifesto. J Ecol 102:275–301. https://doi.org/10.1111/1365-2745.12211

    Article  Google Scholar 

  66. Reyer C, Lasch-Born P, Suckow F, Gutsch M, Murawski A, Pilz T (2014) Projections of regional changes in forest net primary productivity for different tree species in Europe driven by climate change and carbon dioxide. Ann For Sci 71:211–225. https://doi.org/10.1007/s13595-013-0306-8

    Article  Google Scholar 

  67. Rosseel Y (2012) lavaan: an R package for structural equation modeling. J Stat Softw 48:1–36

    Article  Google Scholar 

  68. Roumet C, Birouste M, Picon-Cochard C, Ghestem M, Osman N, Vrignon-Brenas S, Cao KF, Stokes A (2016) Root structure-function relationships in 74 species: evidence of a root economics spectrum related to carbon economy. New Phytol 210(3):815–826

    Article  PubMed  Google Scholar 

  69. Scharnweber T, Manthey M, Criegee C, Bauwe A, Schröder C (2011) Drought matters—declining precipitation influences growth of Fagus sylvatica L. and Quercus robur L. in north eastern Germany. For Ecol Manag 262:947–961. https://doi.org/10.1016/j.foreco.2011.05.026

    Article  Google Scholar 

  70. Steubing L, Fangmeier A (1992) Pflanzenökologisches Praktikum. Parey Verlag, Berlin

    Google Scholar 

  71. Temperton VM, Millard P, Jarvis PG (2003) Does elevated atmospheric carbon dioxide affect internal nitrogen allocation in the temperate trees Alnus glutinosa and Pinus sylvestris? Glob Change Biol 9:286–294. https://doi.org/10.1046/j.1365-2486.2003.00568.x

    Article  Google Scholar 

  72. Thornley JHM (1972) A balanced quantitative model for root: shoot ratios in vegetative plants. Ann Bot 36:431–441

    Article  Google Scholar 

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

    Book  Google Scholar 

  74. Von Oheimb G, Härdtle W, Naumann PS, Westphal C, Assmann T, Meyer H (2008) Long-term effects of historical heathland farming on soil properties of forest ecosystems. For Ecol Manag 255:1984–1993. https://doi.org/10.1016/j.foreco.2007.12.021

    Article  Google Scholar 

  75. Von Oheimb G, Härdtle W, Eckstein D, Engelke H-H, Hehnke T, Wagner B, Fichtner A (2014) Does forest continuity enhance the resilience of trees to environmental change? PLoS ONE 9(12):1–18. https://doi.org/10.1371/journal.pone.0113507

    CAS  Article  Google Scholar 

  76. Wagner S, Collet C, Madsen P, Nakashizuka T, Nyland RD, Sagheb-Talebi K (2010) Beech regeneration research: from ecological to silvicultural aspects. For Ecol Manag 259:2172–2182. https://doi.org/10.1016/j.foreco.2010.02.029

    Article  Google Scholar 

  77. Weemstra M, Mommer L, Visser EJW, van Ruijven J, Kuyper TW, Mohren GMJ, Sterck FJ (2016) Towards a multidimensional root trait framework: a tree root review. New Phytol 211:1159–1169. https://doi.org/10.1111/nph.14003

    Article  PubMed  CAS  Google Scholar 

  78. Williams AP, Allen CD, Macalady AK, Griffin D, Woodhouse CA, Meko DM, Swetman TW, Rauscher SA, Seager R, Grissino-Mayer HD, Dean JS, Cook ER, Gangodagamage C, Cai M, McDowell NG (2013) Temperature as a potent driver of regional forest drought stress and tree mortality. Nat Clim Change 3:292–297. https://doi.org/10.1038/nclimate1693

    Article  Google Scholar 

  79. Yuan ZY, Chen HYH (2010) Fine root biomass, production, turnover rates, and nutrient contents in boreal forest ecosystems in relation to species, climate, fertility, and stand age: literature review and meta-analyses. Crit Rev Plant Sci 29:204–221. https://doi.org/10.1080/07352689.2010.483579

    Article  CAS  Google Scholar 

  80. Zang C, Hartl-Meier C, Dittmar C, Rothe A, Menzel A (2014) Patterns of drought tolerance in major European temperate forest trees: climatic drivers and levels of variability. Glob Change Biol 20:3767–3779. https://doi.org/10.1111/gcb.12637

    Article  Google Scholar 

  81. 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  PubMed Central  CAS  Google Scholar 

  82. Zimmermann J, Hauck M, Dulamsuren C, Leuschner C (2015) Climate warming-related growth decline affects Fagus sylvatica, but not other broad-leaved tree species in central European mixed forests. Ecosystems 18:560–572. https://doi.org/10.1007/s10021-015-9849-x

    Article  CAS  Google Scholar 

  83. Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New York

    Book  Google Scholar 

  84. Zuur AF, Ieno EN, Elphick CS (2010) A protocol for data exploration to avoid common statistical problems. Methods Ecol Evol 1:3–14. https://doi.org/10.1111/j.2041-210X.2009.00001.x

    Article  Google Scholar 

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Acknowledgements

We thank the local forest owners for allowing us to take increment cores and are grateful to Mechthild Stange, Thomas Niemeyer and Rafael Weidlich for assisting with fine root and soil analyses. KM was funded by a doctoral fellowship from the German Federal Environmental Foundation (DBU; AZ20013/279). We thank the reviewers and the editor for their constructive comments.

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AF, WH, GvO, CL and VMT designed the research; DH designed methodology for the root sampling and analysis; KM collected and compiled the data; KM and AF analysed the data; DH, BD and KJ assisted with the interpretation and discussion of root data; KM wrote the first draft of the manuscript. All authors substantially contributed to revisions and gave final approval for publication.

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Correspondence to Katharina Mausolf.

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Communicated by Hakan Wallander.

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Mausolf, K., Härdtle, W., Jansen, K. et al. Legacy effects of land-use modulate tree growth responses to climate extremes. Oecologia 187, 825–837 (2018). https://doi.org/10.1007/s00442-018-4156-9

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Keywords

  • Climate change
  • European beech
  • Fine roots
  • Forest continuity
  • Plant–climate interactions