Advertisement

Alpine Botany

, Volume 129, Issue 2, pp 175–183 | Cite as

Are mountaintops climate refugia for plants under global warming? A lesson from high-mountain oaks in tropical rainforest

  • Hong-Hu Meng
  • Shi-Shun Zhou
  • Xiao-Long Jiang
  • Paul F. Gugger
  • Lang Li
  • Yun-Hong Tan
  • Jie LiEmail author
Short Communication

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.

Keywords

Changing climate Climate refugia Mountaintops Global warming Biodiversity Oak trees 

Notes

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 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.

Compliance with ethical standards

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.

Supplementary material

35_2019_226_MOESM1_ESM.docx (20 kb)
Appendix S1. The fossil records of the high-mountain oaks (DOCX 19 kb)
35_2019_226_MOESM2_ESM.docx (19 kb)
Appendix S2. Environmental variables and percent contribution to construct species potential distributions used in this study (DOCX 19 kb)

References

  1. 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 45:977–985CrossRefGoogle Scholar
  2. 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 24:563–579CrossRefGoogle Scholar
  3. Bennett KD, Provan J (2008) What do we mean by ‘refugia’? Quat Sci Rev 27:2449–2455CrossRefGoogle Scholar
  4. Birks HJB, Willis KJ (2008) Alpines, trees, and refugia in Europe. Plant Ecol Divers 1:147–160CrossRefGoogle Scholar
  5. Chen IC, Hill JK, Ohlemüller R, Roy DB, Thomas CD (2011) Rapid range shifts of species associated with high levels of climate warming. Science 333:1024–1026CrossRefGoogle Scholar
  6. Davis MB (1976) Pleistocene biogeography of temperate deciduous forests. Geosci Man 13:13–26Google Scholar
  7. Davis MB, Shaw RG (2001) Range shifts and adaptive responses to Quaternary climate change. Science 292:673–679CrossRefGoogle Scholar
  8. 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, BaselGoogle Scholar
  9. Dillon ME, Wang G, Huey RB (2010) Global metabolic impacts of recent climate warming. Nature 467:704–707CrossRefGoogle Scholar
  10. 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 44:294–307CrossRefGoogle Scholar
  11. 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 2:619–622CrossRefGoogle Scholar
  12. 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 7:1688PubMedPubMedCentralGoogle Scholar
  13. 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 204:37–54CrossRefGoogle Scholar
  14. Gentili R, Badola HK, Birks HJB (2015) Alpine biodiversity and refugia in changing climate. Biodibersity 16:163–195Google Scholar
  15. Ghazoul J, Sheil D (2010) Tropical rain forest ecology: diversity & conservation. Oxford University Press, New York, p 309 (also see color plate 10) Google Scholar
  16. 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 21:1651–1671CrossRefGoogle Scholar
  17. 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 22:3598–3612CrossRefGoogle Scholar
  18. Hampe A, Petit RJ (2005) Conserving biodiversity under climate change: the rear edge matters. Ecol Lett 8:461–467CrossRefGoogle Scholar
  19. Hanley JA, McNeil BJ (1982) The meaning and use of the area under a receiver operating characteristic (ROC) curve. Radiology 143:29–36CrossRefGoogle Scholar
  20. Hewitt GM (1996) Some genetic consequences of ice ages, and their role in divergence and speciation. Biol J Linn Soc 58:247–276CrossRefGoogle Scholar
  21. Hewitt GM (2000) The genetic legacy of the Quaternary ice ages. Nature 405:907–913CrossRefGoogle Scholar
  22. Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A (2005) Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 25:1965–1978CrossRefGoogle Scholar
  23. Huang CJ, Zhang YT, Bartholomew B (1999) Fagaceae. In: Wu ZY, Raven PH (eds) Flora of China. Science Press, Beijing, pp 314–400Google Scholar
  24. 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 61:1354–1364Google Scholar
  25. Huntley B, Birks HJB (1983) An atlas of past and present pollen maps for Europe: 0–13,000 years ago. Cambridge University Press, CambridgeGoogle Scholar
  26. 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 12:104CrossRefGoogle Scholar
  27. Kelly AE, Goulden ML (2008) Rapid shifts in plant distribution with recent climate change. Pro Natl Acad Sci 105:11823–11826CrossRefGoogle Scholar
  28. 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 21:393–404CrossRefGoogle Scholar
  29. Knowles LL (2001) Did the Pleistocene glaciations promote divergence? Tests of explicit refugial models in montane grasshopprers. Mol Ecol 10:691–701CrossRefGoogle Scholar
  30. 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 320:1768–1771CrossRefGoogle Scholar
  31. 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 45:1334–1444CrossRefGoogle Scholar
  32. McLachlan JS, Clark JS, Manos PS (2005) Molecular indicators of tree migration capacity under rapid climate change. Evolution 86:2088–2098Google Scholar
  33. 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 26:3276–3294CrossRefGoogle Scholar
  34. 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 28:525–537CrossRefGoogle Scholar
  35. Menitsky YL (1984) Oaks of Asia. Duby Azii, Nauka, pp 89–97Google Scholar
  36. 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 32:65–74CrossRefGoogle Scholar
  37. 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 185:332–342CrossRefGoogle Scholar
  38. 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 336:353–355CrossRefGoogle Scholar
  39. 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 300:1563–1565CrossRefGoogle Scholar
  40. Petit RJ, Hu FS, Dick CW (2008) Forests of the past: a window to future changes. Science 320:1450–1452CrossRefGoogle Scholar
  41. Phillips SJ, Anderson RP, Schapire RE (2006) Maximum entropy modeling of species geographic distributions. Ecol Model 190:231–259CrossRefGoogle Scholar
  42. 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 16:1258–1266CrossRefGoogle Scholar
  43. 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 115:1848–1853CrossRefGoogle Scholar
  44. 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 54:475–478CrossRefGoogle Scholar
  45. 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 17:186–193CrossRefGoogle Scholar
  46. 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 444:269–279CrossRefGoogle Scholar
  47. 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 277:661–671CrossRefGoogle Scholar
  48. 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 6:495–504CrossRefGoogle Scholar
  49. 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 43:1126–1133Google Scholar
  50. R Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org/
  51. Thuiller W, Lavorel S, Araújo MB, Sykes MT, Prentice IC (2005) Climate change threats to plant diversity in Europe. Proc Natl Acad Sci 102:8245–8250CrossRefGoogle Scholar
  52. Willis KJ, Whittaker RJ (2000) The refugial debate. Science 287:1406–1407CrossRefGoogle Scholar
  53. 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 43:2261–2273CrossRefGoogle Scholar
  54. 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 37:1184–1193CrossRefGoogle Scholar
  55. 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 7:1–34Google Scholar
  56. Zhou ZK, Pu CX, Chen WY (2003) Relationships between the distributions of Quercus Sect. Heterobalanus (Fagaceae) and uplift of Himalayas. Adv Earth Sci 18:884–890Google Scholar

Copyright information

© Swiss Botanical Society 2019

Authors and Affiliations

  1. 1.Plant Phylogenetics and Conservation Group, Center for Integrative Conservation, Xishuangbanna Tropical Botanical GardenChinese Academy of SciencesKunmingChina
  2. 2.Specimens and Germplasm Conservation Center, Center for Integrative Conservation, Xishuangbanna Tropical Botanical GardenChinese Academy of SciencesMenglunChina
  3. 3.Shanghai Chenshan Plant Science Research CenterChinese Academy of SciencesShanghaiChina
  4. 4.Appalachian LaboratoryUniversity of Maryland Center for Environmental ScienceFrostburgUSA
  5. 5.Plant Diversity and Conservation Group, Center for Integrative Conservation, Xishuangbanna Tropical Botanical GardenChinese Academy of SciencesMenglunChina
  6. 6.Southeast Asia Biodiversity Research InstituteChinese Academy of SciencesNay Pyi TawMyanmar

Personalised recommendations