Ongoing climate change is expected to shift tree species distribution and therefore affect forest biodiversity and ecosystem services. To assess and project tree distributional shifts, researchers may compare the distribution of juvenile and adult trees under the assumption that differences between tree life stages reflect distributional shifts triggered by climate change. However, the distribution of tree life stages could differ within the lifespan of trees, therefore, we hypothesize that currently observed distributional differences could represent shifts over ontogeny as opposed to climatically driven changes. Here, we test this hypothesis with data from 1435 plots resurveyed after more than three decades across the Western Carpathians. We compared seedling, sapling and adult distribution of 12 tree species along elevation, temperature and precipitation gradients. We analyzed (i) temporal shifts between the surveys and (ii) distributional differences between tree life stages within both surveys. Despite climate warming, tree species distribution of any life stage did not shift directionally upward along elevation between the surveys. Temporal elevational shifts were species specific and an order of magnitude lower than differences among tree life stages within the surveys. Our results show that the observed range shifts among tree life stages are more consistent with ontogenetic differences in the species' environmental requirements than with responses to recent climate change. The distribution of seedlings substantially differed from saplings and adults, while the distribution of saplings did not differ from adults, indicating a critical transition between seedling and sapling tree life stages. Future research has to take ontogenetic differences among life stages into account as we found that distributional differences recently observed worldwide may not reflect climate change but rather the different environmental requirements of tree life stages.

Department of GIS and Remote Sensing Institute of Botany The Czech Academy of Sciences Zámek 1 CZ 252 43 Průhonice Czech Republic

Department of Vegetation Ecology Institute of Botany The Czech Academy of Sciences Lidická 25 27 CZ 602 00 Brno Czech Republic

Faculty of Forestry Technical University in Zvolen T G Masaryka 24 SK 960 53 Zvolen Slovak Republic

Forest Research Institute Zvolen National Forest Centre T G Masaryka 22 SK 960 52 Zvolen Slovak Republic

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Akselsson C, Ardö J, Sverdrup H. Critical loads of acidity for forest soils and relationship to forest decline in the northern Czech Republic. Environmental Monitoring and Assessment. 2004;98:363–79. PubMed

Allen CD, Macalady AK, Chenchouni H, et al. A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests. Forest Ecology and Management. 2010;259:660–684.

Bell DM, Bradford JB, Lauenroth WK. Mountain landscapes offer few opportunities for high elevation tree species migration. Global Change Biology. 2014;20:1441–1451. PubMed

Bell DM, Bradford JB, Lauenroth WK. Early indicators of change: divergent climate envelopes between tree life stages imply range shifts in the western United States. Global Ecology and Biogeography. 2013;23:168–180.

Benavides R, Rabasa SG, Granda E, et al. Direct and indirect effects of climate on demography and early growth of Pinus sylvestris at the rear edge: changing roles of biotic and abiotic factors. PloS ONE. 2013;8:e59824. PubMed PMC

Bennett AC, McDowell NG, Allen CD, Anderson-Teixeira KJ. Larger trees suffer most during drought in forests worldwide. Nature Plants. 2015;1:15139. PubMed

Bertrand R, GJ, Gégout JC, Bontemps J. Niches of temperate tree species converge towards nutrient-richer conditions over ontogeny. Oikos. 2011;120:1479–1488.

Bodin J, Badeau V, Bruno E, Cluzeau C, Moisselin J-M, Walther G-R, Dupouey J-L. Shifts of forest species along an elevational gradient in Southeast France: climate change or stand maturation? Journal of Vegetation Science. 2012;24:269–283.

Boisvert-Marsh L, Périé C, de Blois S. Shifting with climate? Evidence for recent changes in tree species distribution at high latitudes. Ecosphere. 2014;5:1–33.

Bošeľa M, Petráš R, Sitková Z, et al. Possible causes of the recent rapid increase in the radial increment of silver fir in the Western Carpathians. Environmental Pollution. 2014;184:211–221. PubMed

Brasier CM. Ophiostoma novo-ulmi sp. nov., causative agent of current Dutch elm disease pandemics. Mycopathologia. 1991;115:151–161.

Breshears DD, Cobb NS, Rich PM, et al. Regional vegetation die-off in response to global-change-type drought. Proceedings of the National Academy of Sciences of the United States of America. 2005;102:15144–15148. PubMed PMC

Brewer S, Cheddadi R, de Beaulieu JL, et al. The spread of deciduous Quercus throughout Europe since the last glacial period. Forest Ecology and Management. 2002;156:27–48.

Büntgen U, Tegel W, Kaplan JO, et al. Placing unprecedented recent fir growth in a European-wide and Holocene-long context. Frontiers in Ecology and the Environment. 2014;12:100–106.

Chen I, Hill JK, Ohlemüller R, Roy DB, Thomas CD. Rapid range shifts of species of climate warming. Science. 2011;333:1024–1026. PubMed

Clark JS, Bell DM, Hersh MH, et al. Individual-scale variation, species-scale differences: inference needed to understand diversity. Ecology Letters. 2011;14:1273–1287. PubMed

Coudun C, Gégout JC. Ecological behaviour of herbaceous forest species along a pH gradient: a comparison between oceanic and semicontinental regions in northern France. Global Ecology and Biogeography. 2005;14:263–270.

Crimmins S, Dobrowski S, Greenberg J, Abatzoglou J, Mynsberge AR. Changes in climatic water balance drive downhill shifts in plant species’ optimum elevations. Science. 2011;331:324–327. PubMed

Davis MB, Shaw RG. Range shifts and adaptive responses to Quaternary climate change. Science. 2001;292:673–679. PubMed

De Frenne P, Rodríguez-Sánchez F, Coomes DA, et al. Microclimate moderates plant responses to macroclimate warming. Proceedings of the National Academy of Sciences of the United States of America. 2013;110:18561–18565. PubMed PMC

Diekmann M, Lawesson JE. Shifts in ecological behaviour of herbaceous forest species along a transect from northern central to north Europe. Folia Geobotanica. 1999;34:127–141.

Dobrowski SZ, Swanson AK, Abatzoglou JT, Holden ZA, Safford HD, Schwartz MK, Gavin DG. Forest structure and species traits mediate projected recruitment declines in western US tree species. Global Ecology and Biogeography. 2015 doi: 10.1111/geb.12302. DOI

Ehrlén J, Morris WF. Predicting changes in the distribution and abundance of species under environmental change. Ecology Letters. 2015;18:303–314. PubMed PMC

Eriksson O. Ontogenetic niche shifts and their implications for recruitment in three clonal Vaccinium shrubs: Vaccinium myrtillus, Vaccinium vitis-idaea, and Vaccinium oxycoccos. Canadian Jounal of Botany. 2002;80:635–641.

Ewald J. Vegetation databases provide a close-up on altitudinal tree species distribution in the Bavarian Alps. In: Dengler J, Oldeland J, Jansen F, Chytrý M, Ewald J, Finckh M, Glöckler F, Lopez-Gonzalez G, Peet RK, Schaminée JHJ, editors. Vegetation databases for the 21st century, Biodiversity & Ecology. Vol. 4. 2012. pp. 41–48.

Faško P, Lapin M, Pecho J. 20-year extraordinary climatic period in Slovakia. Meteorologický časopis – Meterological journal. 2008;11:99–105.

Faško P, Štastný P. Landscape Atlas of the Slovak Republic. Ministry of Environment of the Slovak Republic, Bratislava, Slovak Environmental Agency; Banská Bystrica: 2002. Mean annual precipitation totals; p. 99.

Gehrig-Fasel J, Guisan A, Zimmermann NE. Tree line shifts in the Swiss Alps: Climate change or land abandonment? Journal of Vegetation Science. 2007;18:571–582.

Gibson-Reinemer DK, Rahel FJ. Inconsistent range shifts within species highlight idiosyncratic responses to climate warming. PLoS ONE. 2015;10:e0132103. PubMed PMC

Gottfried M, Pauli H, Futschik A, et al. Continent-wide response of mountain vegetation to climate change. Nature Climate Change. 2012;2:111–115.

Gray RKS, Grist NR. Natural regeneration of limes (Tilia spp.) in Scotland: Locally widespread and more numerous in 1999. Glasgow Naturalist. 2000;23:13–16.

Grytnes JA, Kapfer J, Jurasinski G, et al. Identifying the driving factors behind observed elevational range shifts on European mountains. Global Ecology and Biogeography. 2014;23:876–884.

Hédl R, Kopecký M, Komárek J. Half a century of succession in a temperate oakwood: from species-rich community to mesic forest. Diversity and Distributions. 2010;16:267–276.

Hlásny T, Turčáni M. Persisting bark beetle outbreak indicates the unsustainability of secondary Norway spruce forests: Case study from Central Europe. Annals of Forest Science. 2013;70:481–491.

Honnay O, Verheyen K, Butaye J, Jacquemyn H, Bossuyt B, Hermy M. Possible effects of habitat fragmentation and climate change on the range of forest plant species. Ecology Letters. 2002;5:525–530.

Hothorn T, Hornik K, van de Wiel M, Zeileis A. Implementing a class of permutation tests: The coin package. Journal of Statistical Software. 2008;28:1–23. PubMed

Ibáñez I, Clark JS, Dietze MC. Estimating colonization potential of migrant tree species. Global Change Biology. 2009;15:1173–1188.

Jamnický J. Vplyv grafiózy na zastúpenie brestov v oblasti slovenských nížin a pahorkatín. Lesnícky časopis. 1976;22:399–406.

Kelly AE, Goulden ML. Rapid shifts in plant distribution with recent climate change. Proceedings of the National Academy of Sciences of the United States of America. 2008;105:11823–11826. PubMed PMC

Kopecký M, Hédl R, Szabó P. Non-random extinctions dominate plant community changes in abandoned coppices. Journal of Applied Ecology. 2013;50:79–87. PubMed PMC

Körner C. Alpine plant life: functional plant ecology of high mountain ecosystems. Springer Science & Business Media; Heidelberg: 2003.

Lenoir J, Gégout J-C, Guisan A, et al. Going against the flow: potential mechanisms for unexpected downslope range shifts in a warming climate. Ecography. 2010;33:295–303.

Lenoir J, Gégout JC, Marquet PA, de Ruffray P, Brisse H. A significant upward shift in plant species optimum elevation during the 20th century. Science. 2008;320:1768–1771. PubMed

Lenoir J, Gégout J-C, Pierrat J-C, Bontemps J-D, Dhôte J-F. Differences between tree species seedling and adult altitudinal distribution in mountain forests during the recent warm period (1986–2006) Ecography. 2009;32:765–777.

Lenoir J, Svenning J-C. Climate-related range shifts - a global multidimensional synthesis and new research directions. Ecography. 2015;38:15–38.

Lloret F, Peñuelas J, Prieto P, Llorens L, Estiarte M. Plant community changes induced by experimental climate change: Seedling and adult species composition. Perspectives in Plant Ecology, Evolution and Systematics. 2009;11:53–63.

Van Mantgem PJ, Stephenson NL, Byrne JC, et al. Widespread increase of tree mortality rates in the western United States. Science. 2009;323:521–524. PubMed

Madrigal-González J, García-Rodríguez JA, Zavala MA. Shrub encroachment shifts the bioclimatic limit between marcescent and sclerophyllous oaks along an elevation gradient in west-central Spain. Journal of Vegetation Science. 2014;25:514–524.

Melo M, Lapin M, Kapolková H, Pecho J. Climate Trends in the Slovak Part of the Carpathians. In: Kozak J, Ostapowicz K, Bytnerowicz A, Wyżga B, editors. The Carpathians: Integrating Nature and Society Towards Sustainability. Springer-Verlag; Berlin Heidelberg: 2013. pp. 131–150.

Mérian P, Lebourgeois F. Size-mediated climate–growth relationships in temperate forests: a multi-species analysis. Forest Ecology and Management. 2011;261:1382–1391.

Miriti MN. Ontogenetic shift from facilitation to competition in a desert shrub. Journal of Ecology. 2006;94:973–979.

Monleon VJ, Lintz HE. Evidence of tree species’ range shifts in a complex landscape. PLoS ONE. 2015;10:e0118069. PubMed PMC

Nakashizuka T. Species coexistence in temperate, mixed, deciduous forests. Trends in Ecology and Evolution. 2001;16:205–210. PubMed

Niinemets Ü. The controversy over traits conferring shade-tolerance in trees: ontogenetic changes revisited. Journal of Ecology. 2006;94:464–470.

Pearman PB, Guisan A, Broennimann O, Randin CF. Niche dynamics in space and time. Trends in Ecology and Evolution. 2008;23:149–158. PubMed

Petritan MA, Von Lupke B, Petritan IC. Effects of shade on growth and mortality of maple (Acer pseudoplatanus), ash (Fraxinus excelsior) and beech (Fagus sylvatica) saplings. Forestry. 2007;80:397–412.

Pigott CD, Huntley JP. Factors controlling the distribution of Tilia cordata at the northern limits of its geographical range. III. Nature and causes of seed sterility. New Phytologist. 1981;87:817–839.

Rabasa SG, Granda E, Benavides R, et al. Disparity in elevational shifts of European trees in response to recent climate warming. Global Change Biology. 2013;19:2490–2499. PubMed

Radoglou K, Dobrowolska D, Spyroglou G, Nicolecu VN. A review on the ecology and silviculture of limes. (Tilia cordata Mill., Tilia platyphyllos Scop. and Tilia tomentosa Moench.) in Europe. Die Bodenkultur. 2008;60:1–29.

Silvertown J. Plant coexistence and the niche. Trends in Ecology & Evolution. 2004;19:605–611.

Šťastný P, Nieplová E, Melo M. Landscape Atlas of the Slovak Republic. Vol. 98. Ministry of Environment of the Slovak Republic, Bratislava, Slovak Environmental Agency; Banská Bystrica: 2002. Mean annual air temperature.

Štěpánek P, Zahradníček P, Huth R. Interpolation techniques used for data quality control and calculation of technical series: an example of Central European daily time series. Idöjárás. 2011;115:87–98.

Stevens JT, Stafford HD, Harrison S, Latimer AM. Forest disturbance accelerates thermophilization of understorey plant communities. Journal of Ecology. 2015;103:1253–1263.

Stohlgren TJ, Bachand RR, Onami Y, Binkley D. Species-environment relationships and vegetation patterns: effects of spatial scale and tree life-stage. Plant Ecology. 1998;135:215–228.

Urbieta IR, García LV, Zavala MA, Marañón T. Mediterranean pine and oak distribution in southern Spain: Is there a mismatch between regeneration and adult distribution? Journal of Vegetation Science. 2011;22:18–31.

Urli M, Delzon S, Eyermann A, Couallier V, García-Valdés R, Zavala MA, Porté AJ. Inferring shifts in tree species distribution using asymmetric distribution curves: a case study in the Iberian mountains. Journal of Vegetation Science. 2014;25:147–159.

Valladares F, Niinemets Ü. Shade tolerance, a key plant feature of complex nature and consequences. Annual Review of Ecology, Evolution, and Systematics. 2008;39:237–257.

Verheyen K, Baeten L, De Frenne P, et al. Driving factors behind the eutrophication signal in understorey plant communities of deciduous temperate forests. Journal of Ecology. 2012;100:352–365.

Vitasse Y, Hoch G, Randin CF, Lenz A, Kollas C, Körner C. Tree recruitment of European tree species at their current upper elevational limits in the Swiss Alps. Journal of Biogeography. 2012;39:1439–1449.

Vitasse Y, Lenz A, Hoch G, Körner C. Earlier leaf-out rather than difference in freezing resistance puts juvenile trees at greater risk of damage than adult trees. Journal of Ecology. 2014;102:981–988.

Vladovič J, Merganič J, Máliš F, et al. The response of forest vegetation diversity to changes in edaphic-climatic conditions in Slovakia. Technical University in Zvolen; 2014.

Wiens JJ, Graham CH. Niche conservatism: integrating evolution, ecology, and conservation biology. Annual Review of Ecology, Evolution, and Systematics. 2005;36:519–539.

Wild J, Kopecký M, Svoboda M, Zenáhlíková J, Edwards-Jonášová M, Herben T. Spatial patterns with memory: tree regeneration after stand-replacing disturbance in Picea abies mountain forests. Journal of Vegetation Science. 2014;25:1327–1340.

Woodall CW, Oswalt CM, Westfall JA, Perry CH, Nelson MD, Finley AO. An indicator of tree migration in forests of the eastern United States. Forest Ecology and Management. 2009;257:1434–1444.

Woodall CW, Zhu K, Westfall JA, Oswalt CM, D’Amato WA, Walters BF, Lintz HE. Assessing the stability of tree ranges and influence of disturbance in eastern US forests. Forest Ecology and Management. 2013;291:172–180.

Yamamoto SI. Forest gap dynamics and tree regeneration. Journal of Forest Research. 2000;5:223–229.

Young TP, Petersen DA, Clary JJ. The ecology of restoration: historical links, emerging issues and unexplored realms. Ecology Letters. 2005;8:662–673.

Zhu K, Woodall CW, Clark JS. Failure to migrate: lack of tree range expansion in response to climate change. Global Change Biology. 2012;18:1042–1052.

Zhu K, Woodall CW, Ghosh S, Gelfand AE, Clark JS. Dual impacts of climate change: forest migration and turnover through life history. Global Change Biology. 2013;20:251–264. PubMed