[en] In tropical Africa, evidence of widely distributed genera transcending biomes or habitat boundaries has been reported. The evolutionary processes that allowed these lineages to disperse and adapt into new environments are far from being resolved. To better understand these processes, we propose an integrated approach, based on the eco-physio-morphological traits of two sister species with adjacent distributions along a rainfall gradient.
We used wood anatomical traits, plant hydraulics (vulnerability to cavitation, wood volumetric water content and hydraulic capacitance) and growth data from the natural habitat, in a common garden, to compare species with known phylogeny, very similar morphologically, but occupying contrasting habitats: Erythrophleum ivorense (wet forest) and Erythrophleum suaveolens (moist forest and forest gallery).
We identified some slight differences in wood anatomical traits between the two species associated with strong differences in hydraulics, growth, and overall species distribution. The moist forest species, E. suaveolens had narrower vessels and intervessel pits, and higher vessel cell-wall reinforcement than E. ivorense. These traits allow a high resistance to cavitation and a continuous internal water supply of the xylem during water shortage, allowing a higher fitness during drought periods, but limiting growth.
Our results confirm a trade-off between drought tolerance and growth, controlled by subtle adaptations in wood traits, as a key mechanism leading to the niche partitioning between the two Erythrophleum species. The generality of this trade-off and its importance in the diversification of the African tree flora remains to be tested. Our integrated eco-physio-morpho approach could be the way forward.
Disciplines :
Environmental sciences & ecology
Author, co-author :
Gorel, Anaïs ; Université de Liège - Gembloux Agro-Bio Tech > TERRA > Forest is life
Steppe, Kathy; Faculty of Bioscience Engineering, Ghent University > Department of Plants and Crops > Laboratory of Plant Ecology
Beeckman, Hans; Royal Museum for Central Africa > Laboratory for Wood Biology and Xylarium
De Baerdemaeker, Niels; Faculty of Bioscience Engineering, Ghent University > Department of Plants and Crops > Laboratory of Plant Ecology
Doucet, Jean-Louis ; Université de Liège - Gembloux Agro-Bio Tech > TERRA > Forest is life
Daïnou, Kasso ; Université de Liège - ULiège > Ingénierie des biosystèmes (Biose) > Laboratoire de Foresterie des régions trop. et subtropicales
Fayolle, Adeline ; Université de Liège - Gembloux Agro-Bio Tech > TERRA > Forest is life
Language :
English
Title :
Testing the divergent adaptation of two congeneric tree species on a rainfall gradient using eco-physio-morphological traits
Anderegg, W. R. L. (2015). Spatial and temporal variation in plant hydraulic traits and their relevance for climate change impacts on vegetation. New Phytologist 205: 1008–1014. https://doi.org/10.1111/nph.12907
Anderegg, W. R. L., and F. C. Meinzer. (2015). Wood anatomy and plant hydraulics in a changing climate. In U. Hacke (Ed.), Functional and ecological xylem anatomy, pp. 235–253. Springer International Publishing, Cham, Switzerland.
Beeckman, H. (2016). Wood anatomy and trait-based ecology. IAWA Journal 37: 127–151. https://doi.org/10.1163/22941932-20160127
Blach-Overgaard, A., J.-C. Svenning, J. Dransfield, M. Greve, and H. Balslev. (2010). Determinants of palm species distributions across Africa: The relative roles of climate, non-climatic environmental factors, and spatial constraints. Ecography 33: 380–391.
Borchert, R. (1994). Soil and stem water storage determine phenology and distribution of tropical dry forest trees. Ecology 75: 1437–1449. https://doi.org/10.2307/1937467
Borchert, R. (1998). Responses of tropical trees to rainfall seasonality and its long-term changes. Climatic Change 39: 381–393. https://doi.org/10.1023/A:1005383020063
Borchert, R., and W. T. Pockman. (2005). Water storage capacitance and xylem tension in isolated branches of temperate and tropical trees. Tree Physiology 25: 457–466. https://doi.org/10.1093/treephys/25.4.457
Brenes-Arguedas, T., P. D. Coley, and T. A. Kursar. (2009). Pests vs. drought as determinants of plant distribution along a tropical rainfall gradient. Ecology 90: 1751–1761. https://doi.org/10.1890/08-1271.1
Brodersen, C., & McElrone, A. (2013). Maintenance of xylem network transport capacity: A review of embolism repair in vascular plants. Frontiers in Plant Science, 4, 108.
Brodribb, T. J., and H. Cochard. (2009). Hydraulic failure defines the recovery and point of death in water-stressed conifers. Plant Physiology 149: 575–584. https://doi.org/10.1104/pp.108.129783
Choat, B., T. W. Brodie, A. R. Cobb, M. A. Zwieniecki, and N. M. Holbrook. (2006). Direct measurements of intervessel pit membrane hydraulic resistance in two angiosperm tree species. American Journal of Botany 93: 993–1000. https://doi.org/10.3732/ajb.93.7.993
Choat, B., A. R. Cobb, and S. Jansen. (2008). Structure and function of bordered pits: New discoveries and impacts on whole-plant hydraulic function. New Phytologist 177: 608–626. https://doi.org/10.1111/j.1469-8137.2007.02317.x
Choat, B., Jansen, S., Brodribb, T. J., Cochard, H., Delzon, S., Bhaskar, R., … Zanne, A. E. (2012). Global convergence in the vulnerability of forests to drought. Nature, 491, 752–755. https://doi.org/10.1038/nature11688
Choat, B., L. Sack, and N. M. Holbrook. (2007). Diversity of hydraulic traits in nine Cordia species growing in tropical forests with contrasting precipitation. New Phytologist 175: 686–698. https://doi.org/10.1111/j.1469-8137.2007.02137.x
Cornelissen, J. H. C., S. Lavorel, E. Garnier, S. Díaz, N. Buchmann, D. E. Gurvich, … H. Poorter. (2003). A handbook of protocols for standardised and easy measurement of plant functional traits worldwide. Australian Journal of Botany 51: 335–380. https://doi.org/10.1071/BT02124
Currie, D. J., Mittelbach, G. G., Cornell, H. V., Field, R., Guégan, J.-F., Hawkins, B. A., … Turner, J. R. G. (2004). Predictions and tests of climate-based hypotheses of broad-scale variation in taxonomic richness. Ecology Letters, 7, 1121–1134.
De Baerdemaeker, N. J. F., R. L. Salomón, L. De Roo, and K. Steppe. (2017). Sugars from woody tissue photosynthesis reduce xylem vulnerability to cavitation. New Phytologist 216: 720–727. https://doi.org/10.1111/nph.14787
Donkpegan, A. S. L. (2017). Histoire évolutive du complexe Afzelia Smith (Leguminosae - Caesalpinioideae) dans les écosystèmes forestiers et savanicoles en Afrique tropicale. PhD Thesis. Université de Liège, Liège, Belgique.
Donoghue, M. J., and E. J. Edwards. (2014). Biome shifts and niche evolution in plants. Annual Review of Ecology Evolution and Systematics 45: 547–572. https://doi.org/10.1146/annurev-ecolsys-120213-091905
Duminil, J., M. Heuertz, J.-L. Doucet, N. Bourland, C. Cruaud, F. Gavory, … O. J. Hardy. (2010). CpDNA-based species identification and phylogeography: Application to African tropical tree species. Molecular Ecology 19: 5469–5483. https://doi.org/10.1111/j.1365-294X.2010.04917.x
Duminil, J., M. Heuertz, and O. J. Hardy. (2010). Chloroplast DNA polymorphism and phylogeography of a central African tree species widespread in mature rainforests: Greenwayodendron suaveolens (Annonaceae). Tropical Plant Biology 3: 4–13.
Engelbrecht, B. M. J., L. S. Comita, R. Condit, T. A. Kursar, M. T. Tyree, B. L. Turner, and S. P. Hubbell. (2007). Drought sensitivity shapes species distribution patterns in tropical forests. Nature 447: 80–82. https://doi.org/10.1038/nature05747
Epila, J., N. Baerdemaeker, L. L. Vergeynst, W. H. Maes, H. Beeckman, and K. Steppe. (2017). Capacitive water release and internal leaf water relocation delay drought-induced cavitation in African Maesopsis eminii. Tree Physiology 37: 481–490.
Epila, J., W. H. Maes, H. Verbeeck, J. Van Camp, J. B. L. Okullo, and K. Steppe. (2017). Plant measurements on African tropical Maesopsis eminii seedlings contradict pioneering water use behaviour. Environmental and Experimental Botany 135: 27–37. https://doi.org/10.1016/j.envexpbot.2016.12.006
Fayolle, A., Swaine, M. D., Bastin, J.-F., Bourland, N., Comiskey, J. A., Dauby, G., … Plumptre, A. J. (2014). Patterns of tree species composition across tropical African forests. Journal of Biogeography, 6, 364–12.
Gaviria, J., and B. M. J. Engelbrecht. (2015). Effects of drought, pest pressure and light availability on seedling establishment and growth: Their role for distribution of tree species across a tropical rainfall gradient. PLoS ONE 10: e0143955. https://doi.org/10.1371/journal.pone.0143955
Gaviria, J., Turner, B. L., & Engelbrecht, B. M. J. (2017). Drivers of tree species distribution across a tropical rainfall gradient. Ecosphere, 8, e01712.
Gleason, S. M., Westoby, M., Jansen, S., Choat, B., Hacke, U. G., Pratt, R. B., … Zanne, A. E. (2016). Weak tradeoff between xylem safety and xylem-specific hydraulic efficiency across the world's woody plant species. New Phytologist, 209, 123–136. https://doi.org/10.1111/nph.13646
Gorel, A.-P., Steppe, K., Beeckman, H., De Baerdemaeker, N. J. F., Doucet, J.-L., Ligot, G., … Fayolle, A. (2019). Data from: Testing the divergent adaptation of two congeneric tree species on a rainfall gradient using eco-physio-morphological traits. Dryad Digital Repository. https://doi.org/10.5061/dryad.hj0005k
Hacke, U. G., J. S. Sperry, W. T. Pockman, S. D. Davis, and K. A. McCulloh. (2001). Trends in wood density and structure are linked to prevention of xylem implosion by negative pressure. Oecologia 126: 457–461. https://doi.org/10.1007/s004420100628
Hérault, B., B. Bachelot, L. Poorter, V. Rossi, F. Bongers, J. Chave, … C. Baraloto. (2011). Functional traits shape ontogenetic growth trajectories of rain forest tree species: Plant traits shape growth trajectory. Journal of Ecology 99: 1431–1440. https://doi.org/10.1111/j.1365-2745.2011.01883.x
Hijmans, R. J., S. E. Cameron, J. L. Parra, P. G. Jones, and A. Jarvis. (2005). Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology 25: 1965–1978. https://doi.org/10.1002/(ISSN)1097-0088
Holstein, N., and S. S. Renner. (2011). A dated phylogeny and collection records reveal repeated biome shifts in the African genus Coccinia (Cucurbitaceae). BMC Evolutionary Biology 11: 28. https://doi.org/10.1186/1471-2148-11-28
InsideWood. 2004-onwards. Published on the Internet. http://insidewood.lib.ncsu.edu/search [accessed 15 Dec. 2017].
Jones, A., Breuning-Madison, H., Brossard, M., Dampha, A., Deckers, J., Dewitte, O., … Kilsara, M. (2013). Soil atlas of Africa; European Commission. Luxembourg: Publications of the European Union.
Lachenbruch, B., and K. A. McCulloh. (2014). Traits, properties, and performance: How woody plants combine hydraulic and mechanical functions in a cell, tissue, or whole plant. New Phytologist 204: 747–764. https://doi.org/10.1111/nph.13035
Lachenbruch, B., Moore, J. R., & Evans, R. (2011). Radial variation in wood structure and function in woody plants, and hypotheses for its occurrence. In F. C. Meinzer, B. Lachenbruch & T. E. Dawson (Eds.), Size- and age-related changes in tree structure and function. Tree physiology (pp. 121–164). Berlin, Netherlands: Springer Netherlands. https://doi.org/10.1007/978-94-007-1242-3
Lens, F., J. S. Sperry, M. A. Christman, B. Choat, D. Rabaey, and S. Jansen. (2011). Testing hypotheses that link wood anatomy to cavitation resistance and hydraulic conductivity in the genus Acer. New Phytologist 190: 709–723. https://doi.org/10.1111/j.1469-8137.2010.03518.x
Letouzey, R. (1985). Notice de la carte phytogéographique du Cameroun au 1: 500'000.
Li, S., F. Lens, S. Espino, Z. Karimi, M. Klepsch, H. J. Schenk, … S. Jansen. (2016). Intervessel pit membrane thickness as a key determinant of embolism resistance in angiosperm xylem. IAWA Journal 37: 152–171. https://doi.org/10.1163/22941932-20160128
Linder, H. P. (2001). Plant diversity and endemism in sub-Saharan tropical Africa: African phytogeography. Journal of Biogeography 28: 169–182. https://doi.org/10.1046/j.1365-2699.2001.00527.x
Linder, H. P. (2014). The evolution of African plant diversity. Frontiers in Ecology and Evolution, 2, 38.
Maharjan, S. K., L. Poorter, M. Holmgren, F. Bongers, J. J. Wieringa, and W. D. Hawthorne. (2011). Plant functional traits and the distribution of West African rain forest trees along the rainfall gradient: Functional traits affect species distribution. Biotropica 43: 552–561. https://doi.org/10.1111/j.1744-7429.2010.00747.x
Markesteijn, L., and L. Poorter. (2009). Seedling root morphology and biomass allocation of 62 tropical tree species in relation to drought- and shade-tolerance. Journal of Ecology 97: 311–325. https://doi.org/10.1111/j.1365-2745.2008.01466.x
Markesteijn, L., L. Poorter, F. Bongers, H. Paz, and L. Sack. (2011). Hydraulics and life history of tropical dry forest tree species: Coordination of species’ drought and shade tolerance. New Phytologist 191: 480–495. https://doi.org/10.1111/j.1469-8137.2011.03708.x
Markesteijn, L., L. Poorter, H. Paz, L. Sack, and F. Bongers. (2011). Ecological differentiation in xylem cavitation resistance is associated with stem and leaf structural traits: Vulnerability to cavitation of tropical dry forest tree species. Plant, Cell and Environment 34: 137–148. https://doi.org/10.1111/j.1365-3040.2010.02231.x
Mcculloh, K. A., D. M. Johnson, F. C. Meinzer, and D. R. Woodruff. (2014). The dynamic pipeline: Hydraulic capacitance and xylem hydraulic safety in four tall conifer species. Plant, Cell and Environment 37: 1171–1183. https://doi.org/10.1111/pce.12225
Meinzer, F. C., S. A. James, and G. Goldstein. (2004). Dynamics of transpiration, sap flow and use of stored water in tropical forest canopy trees. Tree Physiology 24: 901–909. https://doi.org/10.1093/treephys/24.8.901
Meinzer, F. C., S. A. James, G. Goldstein, and D. Woodruff. (2003). Whole-tree water transport scales with sapwood capacitance in tropical forest canopy trees. Plant, Cell and Environment 26: 1147–1155. https://doi.org/10.1046/j.1365-3040.2003.01039.x
Moles, A. T., and M. Westoby. (2006). Seed size and plant strategy across the whole life cycle. Oikos 113: 91–105. https://doi.org/10.1111/j.0030-1299.2006.14194.x
Morris, H., and S. Jansen. (2016). Secondary xylem parenchyma–from classical terminology to functional traits. IAWA J 37: 364–13. https://doi.org/10.1163/22941932-20160117
Muggeo, V. (2008). Segmented: An R package to fit regression models with broken-line relationships. R News 8: 20–25.
Myers, J. A., and K. Kitajima. (2007). Carbohydrate storage enhances seedling shade and stress tolerance in a neotropical forest. Journal of Ecology 95: 383–395. https://doi.org/10.1111/j.1365-2745.2006.01207.x
O'Brien, E. (1998). Water-energy dynamics, climate, and prediction of woody plant species richness: An interim general model. Journal of Biogeography 25: 379–398. https://doi.org/10.1046/j.1365-2699.1998.252166.x
O'Brien, M. J., B. M. J. Engelbrecht, J. Joswig, G. Pereyra, B. Schuldt, S. Jansen, … C. Macinnis-Ng. (2017). A synthesis of tree functional traits related to drought-induced mortality in forests across climatic zones. Journal of Applied Ecology 54: 1669–1686. https://doi.org/10.1111/1365-2664.12874
Oliva Carrasco, L., S. J. Bucci, D. Di Francescantonio, O. A. Lezcano, P. I. Campanello, F. G. Scholz, … G. Goldstein. (2015). Water storage dynamics in the main stem of subtropical tree species differing in wood density, growth rate and life history traits. Tree Physiology 35: 354–365. https://doi.org/10.1093/treephys/tpu087
Pfautsch, S., M. Harbusch, A. Wesolowski, R. Smith, C. Macfarlane, M. G. Tjoelker, … M. A. Adams. (2016). Climate determines vascular traits in the ecologically diverse genus Eucalyptus. Ecology Letters 19: 240–248. https://doi.org/10.1111/ele.12559
Phillips, N. G., R. Oren, J. Licata, and S. Linder. (2004). Time series diagnosis of tree hydraulic characteristics. Tree Physiology 24: 879–890. https://doi.org/10.1093/treephys/24.8.879
Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D., & R Core Team. (2017). {nlme}: Linear and Nonlinear Mixed Effects Models. Available at: https://CRAN.R-project.org/package=nlme.
Polley, H. W., C. R. Tischler, H. B. Johnson, and J. D. Derner. (2002). Growth rate and survivorship of drought: CO2 effects on the presumed tradeoff in seedlings of five woody legumes. Tree Physiology 22: 383–391. https://doi.org/10.1093/treephys/22.6.383
Poorter, L., and K. Kitajima. (2007). Carbohydrate storage and light requirements of tropical moist and dry forest tree species. Ecology 88: 1000–1011.
Poorter, L., and L. Markesteijn. (2008). Seedling traits determine drought tolerance of tropical tree species. Biotropica 40: 321–331. https://doi.org/10.1111/(ISSN)1744-7429
R Core Team. (2016). R: A language and environment for statistical computing, Vienna, Austria: R Foundation for Statistical Computing. Available from: https://www.R-project.org/
Santiago, L. S., D. Bonal, M. E. De Guzman, and E. Ávila-Lovera. (2016). Drought survival strategies of tropical trees. In G. Goldstein, and L. S. Santiago (Eds.). Tropical tree physiology, pp. 243–258. Springer International Publishing, Cham. https://doi.org/10.1007/978-3-319-27422-5
Santiago, L. S., G. Goldstein, F. C. Meinzer, J. B. Fisher, K. Machado, D. Woodruff, and T. Jones. (2004). Leaf photosynthetic traits scale with hydraulic conductivity and wood density in Panamanian forest canopy trees. Oecologia 140: 543–550. https://doi.org/10.1007/s00442-004-1624-1
Scholz, A., M. Klepsch, Z. Karimi, and S. Jansen. (2013). How to quantify conduits in wood? Frontiers in Plant Science 4: 56.
Scholz, F. G., Phillips, N. G., Bucci, S. J., Meinzer, F. C., & Goldstein, G. (2011). Hydraulic capacitance: Biophysics and functional significance of internal water sources in relation to tree size. In F. C. Meinzer, B. Lachenbruch & T. E. Dawson (Eds.), Size- and age-related changes in tree structure and function. Tree physiology (pp. 341–361). Berlin, Netherlands: Springer Netherlands. https://doi.org/10.1007/978-94-007-1242-3
Sheil, D., A. Salim, J. Chave, J. Vanclay, and W. D. Hawthorne. (2006). Illumination–size relationships of 109 coexisting tropical forest tree species. Journal of Ecology 94: 494–507. https://doi.org/10.1111/j.1365-2745.2006.01111.x
Smith, T., & Huston, M. (1990). A theory of the spatial and temporal dynamics of plant communities. In G. Grabherr, L. Mucina, M. B. Dale & C. J. F. T. Braak (Eds.) Progress in theoretical vegetation science. Advances in vegetation science (pp. 49–69). Berlin, Netherlands: Springer Netherlands. https://doi.org/10.1007/978-94-009-1934-1
Sosef, M. S. M., Dauby, G., Blach-Overgaard, A., van der Burgt, X., Catarino, L., Damen, T., … Couvreur, T. L. (2017). Exploring the floristic diversity of tropical Africa. BMC Biology, 15, 15. https://doi.org/10.1186/s12915-017-0356-8
Sperry, J. S., F. C. Meinzer, and K. A. McCULLOH. (2008). Safety and efficiency conflicts in hydraulic architecture: Scaling from tissues to trees. Plant, Cell and Environment 31: 632–645. https://doi.org/10.1111/j.1365-3040.2007.01765.x
Sterck, F., L. Markesteijn, M. Toledo, F. Schieving, and L. Poorter. (2014). Sapling performance along resource gradients drives tree species distributions within and across tropical forests. Ecology 95: 2514–2525. https://doi.org/10.1890/13-2377.1
Tosso, D. F. (2018). Evolution et adaptation fonctionnelle des arbres tropicaux: le cas du genre Guibourtia Benn. PhD Thesis. Université de Liège, Liège, Belgique.
Tyree, M. T., S. D. Davis, and H. Cochard. (1994). Biophysical perspectives of xylem evolution: Is there a tradeoff of hydraulic efficiency for vulnerability to dysfunction? IAWA Journal 15: 335–360. https://doi.org/10.1163/22941932-90001369
Tyree, M. T., B. M. J. Engelbrecht, G. Vargas, and T. A. Kursar. (2003). Desiccation tolerance of five tropical seedlings in Panama. Relationship to a field assessment of drought performance. Plant Physiology 132: 1439–1447. https://doi.org/10.1104/pp.102.018937
Urli, M., A. J. Porte, H. Cochard, Y. Guengant, R. Burlett, and S. Delzon. (2013). Xylem embolism threshold for catastrophic hydraulic failure in angiosperm trees. Tree Physiology 33: 672–683. https://doi.org/10.1093/treephys/tpt030
Vergeynst, L. L., M. Dierick, J. A. N. Bogaerts, V. Cnudde, and K. Steppe. (2015). Cavitation: A blessing in disguise? New method to establish vulnerability curves and assess hydraulic capacitance of woody tissues. Tree Physiology 35: 400–409. https://doi.org/10.1093/treephys/tpu056
Vergeynst, L. L., M. G. R. Sause, M. A. Hamstad, and K. Steppe. (2015). Deciphering acoustic emission signals in drought stressed branches: The missing link between source and sensor. Frontiers in Plant Science 6: 494.
Westoby, M. (1998). A leaf-height-seed (LHS) plant ecology strategy scheme. Plant and Soil 199: 213–227. https://doi.org/10.1023/A:1004327224729
Westoby, M., D. S. Falster, A. T. Moles, P. A. Vesk, and I. J. Wright. (2002). Plant ecological strategies: Some leading dimensions of variation between species. Annual Review of Ecology and Systematics 33: 125–159. https://doi.org/10.1146/annurev.ecolsys.33.010802.150452
Wheeler, J. K., J. S. Sperry, U. G. Hacke, and N. Hoang. (2005). Inter-vessel pitting and cavitation in woody Rosaceae and other vesselled plants: A basis for a safety versus efficiency trade-off in xylem transport. Plant, Cell and Environment 28: 800–812. https://doi.org/10.1111/j.1365-3040.2005.01330.x
White, F. (1978). The taxonomy, ecology and chorology of African Ebenaceae I. The Guineo-Congolian species. Bulletin du Jardin Botanique National de Belgique 48: 245–358. https://doi.org/10.2307/3667933
White, F. (1983). The vegetation of Africa, a descriptive memoir to accompany the UNESCO/AETFAT/UNSO vegetation map of Africa (3 Plates, Northwestern Africa, Northeastern Africa, and Southern Africa, 1: 5,000,000) United Nations Educational, Scientific and Cultural Organization, Paris.
Wolfe, B. T. (2017). Retention of stored water enables tropical tree saplings to survive extreme drought conditions. Tree Physiology 37: 469–480. https://doi.org/10.1093/treephys/tpx001
Wolfe, B. T., and T. A. Kursar. (2015). Diverse patterns of stored water use among saplings in seasonally dry tropical forests. Oecologia 179: 925–936. https://doi.org/10.1007/s00442-015-3329-z
Zanne, A. E., Lopez-Gonzalez, G., Coomes, D. A., Ilic, J., Jansen, S., Lewis, S. L., … Chave, J. (2009). Global wood density database. Dryad Identifier Httphdl Handle Net10255dryad 235.
Zanne, A. E., Tank, D. C., Cornwell, W. K., Eastman, J. M., Smith, S. A., FitzJohn, R. G., … Beaulieu, J. M. (2013). Three keys to the radiation of angiosperms into freezing environments. Nature, 506, 89–92.
Zuur, A., Ieno, E. N., Walker, N., Saveliev, A. A., & Smith, G. M. (2009). Mixed effects models and extensions in ecology with R. Springer Science & Business Media.
