Global warming is forcing many species to shift their distributions upward, causing consequent changes in the compositions of species that occur at specific locations. This prediction remains largely untested for tropical trees. Here we show, using a database of nearly 200 Andean forest plot inventories spread across more than 33.5° latitude (from 26.8° S to 7.1° N) and 3,000-m elevation (from 360 to 3,360 m above sea level), that tropical and subtropical tree communities are experiencing directional shifts in composition towards having greater relative abundances of species from lower, warmer elevations. Although this phenomenon of ‘thermophilization’ is widespread throughout the Andes, the rates of compositional change are not uniform across elevations. The observed heterogeneity in thermophilization rates is probably because of different warming rates and/or the presence of specialized tree communities at ecotones (that is, at the transitions between distinct habitats, such as at the timberline or at the base of the cloud forest). Understanding the factors that determine the directions and rates of compositional changes will enable us to better predict, and potentially mitigate, the effects of climate change on tropical forests.
Subscribe to Journal
Get full journal access for 1 year
only $3.90 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Tax calculation will be finalised during checkout.
Rent or Buy article
Get time limited or full article access on ReadCube.
All prices are NET prices.
The plot data that support the findings of this study are available from the Red de Bosques (https://redbosques.condesan.org/) upon reasonable request. The list of species included in the analysis with their number of GBIF records after filtering and their estimated thermal optima is available in Supplementary Table 2.
Thuiller, W. Climate change and the ecologist. Nature 448, 550–552 (2007).
Lenoir, J. & Svenning, J. C. Climate-related range shifts - a global multidimensional synthesis and new research directions. Ecography 38, 15–28 (2015).
Feeley, K. J., Rehm, E. M. & Machovina, B. The responses of tropical forest species to global climate change: acclimate, adapt, migrate, or go extinct? Front. Biogeogr. 4, 69–84 (2012).
Chen, I. C., Hill, J. K., Ohlemüller, R., Roy, D. B. & Thomas, C. D. Rapid range shifts of species associated with high levels of climate warming. Science 333, 1024–1026 (2011).
Steinbauer, M. J. et al. Accelerated increase in plant species richness on mountain summits is linked to warming. Nature 556, 231–234 (2018).
Feeley, K. J., Silman, M. R. & Duque, A. Where are the tropical plants? A call for better inclusion of tropical plants in studies investigating and predicting the effects of climate change. Front. Biogeogr. 7, 174–176 (2015).
Perez, T. M., Stroud, J. T. & Feeley, K. J. Thermal trouble in the tropics. Science 351, 1392–1393 (2016).
Colwell, R. K., Brehm, G., Cardelús, C. L., Gilman, A. C. & Longino, J. T. Global warming, elevational range shifts, and lowland biotic attrition in the wet tropics. Science 322, 258–261 (2008).
Telwala, Y., Brook, B. W., Manish, K. & Pandit, M. K. Climate-induced elevational range shifts and increase in plant species richness in a Himalayan biodiversity epicentre. PLoS ONE 8, e57103 (2013).
Jump, A. S., Huang, T.-J. & Chou, C.-H. Rapid altitudinal migration of mountain plants in Taiwan and its implications for high altitude biodiversity. Ecography 35, 204–210 (2012).
Angelo, C. L. & Daehler, C. C. Upward expansion of fire-adapted grasses along a warming tropical elevation gradient. Ecography 36, 551–559 (2013).
Morueta-Holme, N. et al. Strong upslope shifts in Chimborazo’s vegetation over two centuries since Humboldt. Proc. Natl Acad. Sci. USA 112, 12741–12745 (2015).
Feeley, K. J. & Silman, M. R. Keep collecting: accurate species distribution modelling requires more collections than previously thought. Divers. Distrib. 17, 1132–1140 (2011).
Stuart-Smith, R. D., Edgar, G. J., Barrett, N. S., Kininmonth, S. J. & Bates, A. E. Thermal biases and vulnerability to warming in the world’s marine fauna. Nature 528, 88–92 (2015).
Devictor, V. et al. Differences in the climatic debts of birds and butterflies at a continental scale. Nat. Clim. Change 2, 121–124 (2012).
Bertrand, R. et al. Changes in plant community composition lag behind climate warming in lowland forests. Nature 479, 517–520 (2011).
Gottfried, M. et al. Continent-wide response of mountain vegetation to climate change. Nat. Clim. Change 2, 111–115 (2012).
Bush, M. B., Silman, M. R. & Urrego, D. H. 48,000 years of climate and forest change in a biodiversity hot spot. Science 303, 827–829 (2004).
Feeley, K. J. et al. Upslope migration of Andean trees. J. Biogeogr. 38, 783–791 (2011).
Feeley, K. J., Hurtado, J., Saatchi, S., Silman, M. R. & Clark, D. B. Compositional shifts in Costa Rican forests due to climate-driven species migrations. Glob. Change Biol. 19, 3472–3480 (2013).
Duque, A., Stevenson, P. R. & Feeley, K. J. Thermophilization of adult and juvenile tree communities in the northern tropical Andes. Proc. Natl Acad. Sci. USA 112, 10744–10749 (2015).
Báez, S. et al. Large-scale patterns of turnover and basal area change in Andean forests. PLoS ONE 10, e0126594 (2015).
Karger, D. N. et al. Climatologies at high resolution for the earth’s land surface areas. Sci. Data 4, 170122 (2017).
Russell, A. M., Gnanadesikan, A. & Zaitchik, B. Are the Central Andes mountains a warming hot spot? J. Clim. 30, 3589–3608 (2017).
Vuille, M., Franquist, E., Garreaud, R., Lavado Casimiro, W. S. & Cáceres, B. Impact of the global warming hiatus on Andean temperature. J. Geophys. Res. Atmos. 120, 3745–3757 (2015).
Rapp, J. M. & Silman, M. R. Diurnal, seasonal, and altitudinal trends in microclimate across a tropical montane cloud forest. Clim. Res. 55, 17–32 (2012).
Palin, O. F. et al. Termite diversity along an Amazon–Andes elevation gradient, Peru. Biotropica 43, 100–107 (2011).
Fyllas, N. M. et al. Solar radiation and functional traits explain the decline of forest primary productivity along a tropical elevation gradient. Ecol. Lett. 20, 730–740 (2017).
Alexander, J. M., Diez, J. M. & Levine, J. M. Novel competitors shape species’ responses to climate change. Nature 525, 515–518 (2015).
Rehm, E. & Feeley, K. J. Many species risk mountain top extinction long before they reach the top. Front. Biogeogr. 8, e27788 (2016).
Crimmins, S. M., Dobrowski, S. Z., Greenberg, J. A., Abatzoglou, J. T. & Mynsberge, A. R. Changes in climatic water balance drive downhill shifts in plant species’ optimum elevations. Science 331, 324–327 (2011).
Rehm, E. M. & Feeley, K. J. Freezing temperatures as a limit to forest recruitment above tropical Andean treelines. Ecology 96, 1856–1865 (2015).
Bowler, D. & Böhning-Gaese, K. Improving the community-temperature index as a climate change indicator. PLoS ONE 12, e0184275 (2017).
Malizia, A., Easdale, T. A. & Grau, H. R. Rapid structural and compositional change in an old-growth subtropical forest: using plant traits to identify probable drivers. PLoS ONE 8, e73546 (2013).
Carilla, J. & Grau, R. Tendencias sucesionales de los bosques montanos subtropicales del noroeste argentino. Bosque (Valdivia) 32, 97–111 (2011).
McCain, C. M. & Colwell, R. K. Assessing the threat to montane biodiversity from discordant shifts in temperature and precipitation in a changing climate. Ecol. Lett. 14, 1236–1245 (2011).
Myers, N., Mittermeier, R. A., Mittermeier, C. G., da Fonseca, G. A. B. & Kent, J. Biodiversity hotspots for conservation priorities. Nature 403, 853–858 (2000).
Raxworthy, C. J. et al. Extinction vulnerability of tropical montane endemism from warming and upslope displacement: a preliminary appraisal for the highest massif in Madagascar. Glob. Change Biol. 14, 1703–1720 (2008).
Chen, I.-C. et al. Elevation increases in moth assemblages over 42 years on a tropical mountain. Proc. Natl Acad. Sci. USA 106, 1479–1483 (2009).
Forero-Medina, G., Terborgh, J., Socolar, S. J. & Pimm, S. L. Elevational ranges of birds on a tropical montane gradient lag behind warming temperatures. PLoS ONE 6, e28535 (2011).
Feeley, K. J. Moving forward with species distributions. Am. J. Bot. 102, 173–175 (2015).
Svenning, J. C. & Sandel, B. Disequilibrium vegetation dynamics under future climate change. Am. J. Bot. 100, 1266–1286 (2013).
Menéndez, R. et al. Species richness changes lag behind climate change. Proc. R. Soc. B 273, 1465–1470 (2006).
Bertrand, R. et al. Ecological constraints increase the climatic debt in forests. Nat. Commun. 7, 12643 (2016).
Bivand, R. & Yu, D. spgwr: geographically weighted regression. R package version 0.6-32 https://CRAN.R-project.org/package=spgwr (2017).
Dobrowski, S. Z. A climatic basis for microrefugia: the influence of terrain on climate. Glob. Change Biol. 17, 1022–1035 (2011).
Hijmans, R. J. & van Etten, J. raster: geographic analysis and modeling with raster data. R package version 2.0-12 http://CRAN.R-project.org/package=raster (2012).
The Plant List. The plant list: a working list of all plant species. version 1.1 http://www.theplantlist.org/ (2013).
Flann, C. Global Compositae Checklist. https://doi.org/10.15468/g7yhgt (2009).
White, R. ILDIS: The International Legume Database and Information Service. http://www.ildis.org/ (accessed 13 May 2016).
Missouri Botanical Garden. Tropicos. http://www.tropicos.org (accessed 13 May 2016).
USDA NRCS. The PLANTS Database. http://plants.usda.gov (accessed 13 May 2016).
Feeley, K. J. & Silman, M. R. Biotic attrition from tropical forests correcting for truncated temperature niches. Glob. Change Biol. 16, 1830–1836 (2010).
We thank the many individuals and institutions (including the Red de Bosques Andinos, CODESAN, APECO, CONICET and RAINFOR) who are working to protect and understand Andean forests; GBIF and contributing institutions for making collection data publicly available and E. Ortíz for creating the map of plot locations. B.F. and K.J.F. were supported by the US NSF (DEB-1350125) and the Swiss Agency for Development and Cooperation. M.R.S. and W.F.R. were supported by the US NSF (DEB-1754647, DEB-1258112, and EAR-1338694). J.H. was supported by DFG Grants HO3296/2 and HO3296/4. Peruvian plot monitoring was supported by the Blue Moon Fund and the Gordon and Betty Moore Foundation’s Andes to Amazon Program and RAINFOR grant 1656 (coordinated by O. Phillips). A complete list of acknowledgments and funding sources can be found in the Supplementary Information.
Nature thanks A. M. Latimer, J. Lenoir, H. Pauli and the other anonymous reviewer(s) for their contribution to the peer review of this work.
The authors declare no competing interests.
Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Extended data figures and tables
a, The relationship between the mean CTI for each of the Andean forest plots (averaged across all censuses) and the MAT at the plot locations. n = 186, slope = 0.71, R = 0.92, 95% confidence interval = 0.88–0.93, P < 0.001. b, The relationship between the mean plot CTI and plot elevation. n = 186, R = −0.77, 95% confidence interval = −0.82 to −0.7, P < 0.001. c, The relationship between plot MAT and plot elevation. n = 186, R = −0.92, 95% confidence interval = −0.93 to −0.88, P < 0.001. All analyses are two-sided Spearman correlations.
TRplot was compared to the MAT for the Andean forest plots with multiple censuses (n = 64). Each point represents one plot and the size of the point is proportional to the number of censuses. Error bars are 95% confidence intervals based on the linear least-square regressions of the CTI versus census year of each plot. Grey points represent plots with non-significant TRplot values and filled, coloured points represent plots with significant TRplot values; hollow points are plots with only two censuses and for which the significance of the TRplot could therefore not be determined. Positive and negative TRplot are coloured red and blue, respectively.
The thermophilization rates in areas with different warming rates (TRwarm; the annualized change in the mean CTI of all plots within a band of equitable warming rate) were compared to the warming rate. n = 283 plot censuses, assigned to 20 warming bands. The dashed line indicates the mean TRwarm and the coloured shaded area indicates the 95% confidence interval of TRwarm. Positive and negative TRwarm is coloured red and blue, respectively.
Species richness versus MAT in the 1-ha Andean forest plots with multiple censuses. n = 61. Each point represents one plot and the red and blue colours indicate positive and negative TRplot values, respectively. The line shows the linear regression between MAT and species richness. R2 = 0.10, P < 0.05.
The range of thermal optima of co-occurring species versus TRplot in the plots with multiple censuses. n = 64. Each point represents one plot and the red and blue colours represent positive and negative TRplot values, respectively. The line shows the linear regression between the range of the thermal optima of the plots and TRplot. R2 = 0.19, P < 0.001.
Percentage change in absolute basal area per plot for more-thermophilic (species thermal optimum > plot CTI) and less-thermophilic (species thermal optimum < plot CTI) species versus MAT in plots with multiple censuses (n = 64). The more- and less-thermophilic species are coloured red and blue, respectively. Lines show loess regression fits between the percentage change in basal area and MAT, and the shaded areas represent the 95% confidence intervals around the loess regressions.
This file contains extended Acknowledgments.
Supplementary Table 1 in pdf format contains detailed information of the plots included in the analysis such as coordinates, plot size, MAT and CTI. Supplementary Table 2 in pdf format shows the list of the 1720 species included in the analysis, number of GBIF records available after filtering and their estimated Thermal Optima.
About this article
Cite this article
Fadrique, B., Báez, S., Duque, Á. et al. Widespread but heterogeneous responses of Andean forests to climate change. Nature 564, 207–212 (2018). https://doi.org/10.1038/s41586-018-0715-9
- Andean Forests
- Greater Relative Abundance
- Thermal Optimum
- Multiple Census
- Interval Censoring
Trends in Ecology & Evolution (2021)
Little trace of floristic homogenization in peri‐urban Andean secondary forests despite high anthropogenic transformation
Journal of Ecology (2021)
Science of The Total Environment (2021)
Frontiers in Ecology and Evolution (2021)
Demographic Attritions, Elevational Refugia, and the Resilience of Insect Populations to Projected Global Warming
The American Naturalist (2021)