Abstract
Climate refugia are locations where plants are able to survive periods of regionally adverse climate. Such refugia may affect evolutionary processes and the maintenance of biodiversity. Numerous refugia have been identified in the context of Quaternary climate oscillations. With climate warming, there is an increasing need to apply insights from the past to characterize potential future refugia. Mountainous regions, due to the provision of spatially heterogeneous habitats, may contain high biodiversity, particularly important during climate oscillations. Here, we highlight the importance of mountaintops as climate refugia, using the example of high-mountain oaks which are distributed on the ranges of the Himalaya–Hengduan Mountains, and at high elevations in tropical rainforests. The occurrences of cold-adapted high-mountain oaks on mountaintops amidst tropical rainforest indicate that such locations are and will be climate refugia as global warming continues. We examine factors that predict the occurrence of future climate refugia on mountaintops using recognized historical refugia. Future research is needed to elucidate the fine-scale processes and particular geographic locations that buffer species against the rapidly changing climate to guide biodiversity conservation efforts under global warming scenarios.
References
Abeli T, Vamosi JC, Orsenigo S (2018) The importance of marginal population hotspots of cold-adapted species for research on climate change and conservation. J Biogeogr 45:977–985
Alexander JM, Chalmandrier L, Lenoir J, Burgess TI, Essl F, Haider S, Kueffer C, McDougall K, Milbau A, Nunez MA, Pauchard A, Rabitsch W, Rew LJ, Sanders NJ, Pellissier L (2018) Lags in the response of mountain plant communities to climate change. Glob Change Biol 24:563–579
Bennett KD, Provan J (2008) What do we mean by ‘refugia’? Quat Sci Rev 27:2449–2455
Birks HJB, Willis KJ (2008) Alpines, trees, and refugia in Europe. Plant Ecol Divers 1:147–160
Chen IC, Hill JK, Ohlemüller R, Roy DB, Thomas CD (2011) Rapid range shifts of species associated with high levels of climate warming. Science 333:1024–1026
Davis MB (1976) Pleistocene biogeography of temperate deciduous forests. Geosci Man 13:13–26
Davis MB, Shaw RG (2001) Range shifts and adaptive responses to Quaternary climate change. Science 292:673–679
Denk T, Grimm GW, Manos PS, Deng M, Hipp A (2017) An updated infrageneric classification of the oaks: review of previous taxonomic schemes and synthesis of evolutionary patterns. In: Gil-Pelegrín E et al (eds) Oaks physiological ecology. Exploring the functional diversity of genus Quercus L., tree physiology. Springer International Publishing AG, Basel
Dillon ME, Wang G, Huey RB (2010) Global metabolic impacts of recent climate warming. Nature 467:704–707
Du FK, Hou M, Wang W, Mao KS, Hampe A (2016) Phylogeography of Quercus aquifolioides provides novel insights into the Neogene history of a major global hotspot of plant diversity in south-west China. J Biogeogr 44:294–307
Dullinger S, Gattringer A, Thuiller W, Moser D, Zimmermann NE, Guisan A, Hülber K (2012) Extinction debt of high-mountain plants under twenty-first-century climate change. Nat Clim Change 2:619–622
Feng L, Zheng QJ, Qian ZQ, Yang J, Zhang YP, Li ZH, Zhao GF (2016) Genetic structure and evolutionary history of three Alpine Sclerophyllous oaks in East Himalaya–Hengduan Mountains and adjacent regions. Front Plant Sci 7:1688
Gavin DG, Fitzpatrick MC, Gugger PF, Heath KD, Rodríguez-Sánchez F, Dobrowski SZ, Hampe A, Hu FS, Ashcroft MB, Bartlein PJ (2014) Climate refugia: joint inference from fossil records, species distribution models and phylogeography. New Phytol 204:37–54
Gentili R, Badola HK, Birks HJB (2015) Alpine biodiversity and refugia in changing climate. Biodibersity 16:163–195
Ghazoul J, Sheil D (2010) Tropical rain forest ecology: diversity & conservation. Oxford University Press, New York, p 309 (also see color plate 10)
Groves CR, Game ET, Anderson MG, Cross M, Enquist C, Ferdaña Z, Girvetz E, Gondor A, Hall KR, Higgins J (2012) Incorporating climate change into systematic conservation planning. Biodivers Conserv 21:1651–1671
Gugger PF, Ikegami M, Sork VL (2013) Influence of late Quaternary climate change on present patterns of genetic variation in valley oak, Quercus lobata Nee. Mol Ecol 22:3598–3612
Hampe A, Petit RJ (2005) Conserving biodiversity under climate change: the rear edge matters. Ecol Lett 8:461–467
Hanley JA, McNeil BJ (1982) The meaning and use of the area under a receiver operating characteristic (ROC) curve. Radiology 143:29–36
Hewitt GM (1996) Some genetic consequences of ice ages, and their role in divergence and speciation. Biol J Linn Soc 58:247–276
Hewitt GM (2000) The genetic legacy of the Quaternary ice ages. Nature 405:907–913
Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A (2005) Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 25:1965–1978
Huang CJ, Zhang YT, Bartholomew B (1999) Fagaceae. In: Wu ZY, Raven PH (eds) Flora of China. Science Press, Beijing, pp 314–400
Huang HS, Hu JJ, Su T, Zhou ZK (2016) The occurrence of Quercus heqingensis n. sp. and its application to palaeo-CO2 estimates. Chin Sci Bull 61:1354–1364
Huntley B, Birks HJB (1983) An atlas of past and present pollen maps for Europe: 0–13,000 years ago. Cambridge University Press, Cambridge
Jiang XL, Deng M, Li Y (2016) Evolutionary history of subtropical evergreen broad-leaved forest in Yunnan Plateau and adjacent areas: an insight from Quercus schottkyana (Fagaceae). Tree Genet Genomes 12:104
Kelly AE, Goulden ML (2008) Rapid shifts in plant distribution with recent climate change. Pro Natl Acad Sci 105:11823–11826
Keppel G, Niel KPV, Wardell-Johnson GW, Yates CJ, Byrne M, Mucina L, Schut AGT, Hopper SD, Franklin SE (2012) Refugia: identifying and understanding safe havens for biodiversity under climate change. Glob Ecol Biogeogr 21:393–404
Knowles LL (2001) Did the Pleistocene glaciations promote divergence? Tests of explicit refugial models in montane grasshopprers. Mol Ecol 10:691–701
Lenoir J, Gégout JC, Marquet PA, de Ruffray P, Brisse H (2008) A significant upward shift in plant species optimum elevation during the 20th century. Science 320:1768–1771
Liang QL, Xu XT, Mao KS, Wang MC, Wang K, Xi ZX, Liu JQ (2018) Shift in plant distributions in response to climate warming in a biodiversity hotspot, the Hengduan Mountains. J Biogeogr 45:1334–1444
McLachlan JS, Clark JS, Manos PS (2005) Molecular indicators of tree migration capacity under rapid climate change. Evolution 86:2088–2098
Meng HH, Su T, Gao XY, Li J, Jiang XL, Sun H, Zhou ZK (2017) Warm-cold colonization: response of oaks to uplift of the Himalaya–Hengduan Mountains. Mol Ecol 26:3276–3294
Meng HH, ZhouSS Li L, Tan YH, Li JW, Li J (2019) Conflict between biodiversity conservation and economic growth: insight into rare plants in tropical China. Conserv Biodivers 28:525–537
Menitsky YL (1984) Oaks of Asia. Duby Azii, Nauka, pp 89–97
Olson D, Dellasala DA, Noss RF, Strittholt JR, Kass J, Koopman ME, Allnutt TF (2012) Climate change refugia for biodiversity in the Klamath-Siskiyou Ecoregion. Nat Area J 32:65–74
Opgenoorth L, Vendramin GG, Mao K, Miehe G, Miehe S, Liepelt S, Liu J, Ziegenhagen B (2010) Tree endurance on the Tibetan Plateau marks the world’s highest known tree line of the Last Glacial Maximum. New Phytol 185:332–342
Pauli H, Gottfried M, Dullinger S, Abdaladze O, Akhalkatsi M, Benito Alonso JL, Coldea G, Dick J, Erschbamer B, Fernández Calzado R, Ghosn D, Holten JI, Kanka R, Kazakis G, Kollár J, Larsson P, Moiseev P, Moiseev D, Molau U, Molero Mesa J, Nagy L, Pelino G, Puşcaş M, Rossi G, Stanisci A, Syverhuset AO, Theurillat JP, Tomaselli M, Unterluggauer P, Villar L, Vittoz P, Grabherr G (2012) Recent plant diversity changes on Europe’s mountain summits. Science 336:353–355
Petit RJ, Aguinagalde I, de Beaulieu JL, Bittkau C, Brewer S, Cheddadi R, Ennos R, Fineschi S, Grivet D, Lascoux M (2003) Glacial refugia: hotspots but not melting pots of genetic diversity. Science 300:1563–1565
Petit RJ, Hu FS, Dick CW (2008) Forests of the past: a window to future changes. Science 320:1450–1452
Phillips SJ, Anderson RP, Schapire RE (2006) Maximum entropy modeling of species geographic distributions. Ecol Model 190:231–259
Razgour O, Juste J, Ibáñez C, Kiefer A, Rebelo H, Puechmaille SJ, Arlettaz R, Burke T, Dawson DA, Beaumont M (2013) The shaping of genetic variation in edge-of-range populations under past and future climate change. Ecol Lett 16:1258–1266
Rumpf SB, Hülber K, Klonner G, Moser D, Schütz M, Wessely J, Willner W, Zimmermann NE, Dullinger S (2018) Range dynamics of mountain plants decrease with elevation. Proc Natl Acad Sci 115:1848–1853
Shoo LP, Storlie C, Williams YM, Williams SE (2010) Potential for mountaintop boulder fields to buffer species against extreme heat stress under climate change. Int J Biometeorol 54:475–478
Shoo LP, Storlie C, Vanderwal J, Little J, Williams SE (2011) Targeted protection and restoration to conserve tropical biodiversity in a warming world. Glob Change Biol 17:186–193
Song YG, Petitpierre B, Deng M, Wu JP, Kozlowski G (2019) Predicting climate change impacts on the threatened Quercus arbutifolia in montane cloud forests in southern China and Vietnam: conservation implications. For Ecol Manag 444:269–279
Stewart JR, Lister AM, Barnes I, Dalén L (2010) Refugia revisited: individualistic responses of species in space and time. Proc R Soc Lond B Biol Sci 277:661–671
Su T, Spicer RA, Li SH, Xu H, Huang J, Sherlock S, Huang YJ, Li SF, Wang L, Jia LB, Deng WYD, Liu Jia, Deng CL, Zhang ST, Valdes PJ, Zhou ZK (2019) Uplift, climate and biotic changes at the Eocene–Oligocene transition in southeast Tibet. Natl Sci Rev 6:495–504
Sun M, Su T, Zhang SB, Li SF, Anberree-Lebreton J, Zhou ZK (2015) Variations in leaf morphological traits of Quercus guyavifolia (Fagaceae) were mainly influenced by water and ultraviolet irradiation at high elevations on the Qinghai-Tibet Plateau, China. Int J Agric Biol 43:1126–1133
R Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org/
Thuiller W, Lavorel S, Araújo MB, Sykes MT, Prentice IC (2005) Climate change threats to plant diversity in Europe. Proc Natl Acad Sci 102:8245–8250
Willis KJ, Whittaker RJ (2000) The refugial debate. Science 287:1406–1407
Winkler M, Lamprecht A, Steinbauer K, Hülber K, Theurillat JP, Breiner F, Choler P, Siegrun E, Gutiérrez Girón A, Rossi G, Vittoz P, Akhalkatsi M, Bay C, Benito JL, Bergström T, Carranza ML, Corcket E, Dick J, Erschbamer B, Calzado RF, Fosaa AM, Gavilán RG, Ghosn D, Gigauri K, Huber D, Kanka R, Kazakis G, Klipp M, Kollar J, Kudernatsch T, Larsson P, Mallaun M, Michelsen O, Moiseev P, Moiseev D, Molau U, Mesa JM, di Cella UM, Nagy L, Petey M, Pușcaș M, Rixen C, Stanisci A, Suen M, Syverhuset AO, Tomaselli M, Unterluggauer P, Ursu T, Villar L, Gottfried M, Pauli H (2016) The rich sides of mountain summits—a pan-European view of aspect preferences of alpine plants. J Biogeogr 43:2261–2273
Zhang SB, Zhou ZK, Hu H, Xu K (2007) Gas exchange and resource utilization in two alpine oaks at different altitudes in the Hengduan Mountains. Can J For Res 37:1184–1193
Zhou ZK, Wilkinson H, Wu ZY (1994) Taxonomical and evolutionary implications of the leaf anatomy and architecture of Quercus L. subgenus Quercus from China. Cathaya 7:1–34
Zhou ZK, Pu CX, Chen WY (2003) Relationships between the distributions of Quercus Sect. Heterobalanus (Fagaceae) and uplift of Himalayas. Adv Earth Sci 18:884–890
Acknowledgements
Prof. Jürg Stöcklin (Editor-in-Chief of Alpine Botany), Prof. Christian Parisod (Editor of Alpine Botany), and the three anonymous reviewers are gratefully acknowledged for their valuable suggestions and comments. This work is funded by Southeast Asia Biodiversity Research Institute, Chinese Academy of Sciences (Y4ZK111B01); and Youth Innovation Promotion Association, Chinese Academy of Sciences (2018432) to H.-H. Meng.
Author information
Authors and Affiliations
Contributions
HHM and JL conceived the study. HHM, SSZ, LL and YHT conducted field work. XLJ performed data analyses. HHM and PFG wrote the first draft of the manuscript. All of the authors contributed to and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest in relation to this article.
Ethical statement
The authors declare that observance ethical standards.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
35_2019_226_MOESM2_ESM.docx
Appendix S2. Environmental variables and percent contribution to construct species potential distributions used in this study (DOCX 19 kb)
Rights and permissions
About this article
Cite this article
Meng, HH., Zhou, SS., Jiang, XL. et al. Are mountaintops climate refugia for plants under global warming? A lesson from high-mountain oaks in tropical rainforest. Alp Botany 129, 175–183 (2019). https://doi.org/10.1007/s00035-019-00226-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00035-019-00226-2