Plant's-eye view of temperature governs elevational distributions
Language English Country Great Britain, England Media print-electronic
Document type Journal Article
Grant support
GACR17-19376S
Czech Science Foundation - International
31770435
National Natural Science Foundation of China - International
RVO 67985939
Czech Academy of Sciences - International
PubMed
32320507
DOI
10.1111/gcb.15129
Knihovny.cz E-resources
- Keywords
- biophysical traits, carbon stable isotope ratio, decoupling, leaf dry matter content, mountain, oxygen stable isotope ratio, plant height, temperature,
- MeSH
- Oxygen Isotopes MeSH
- Plant Leaves * MeSH
- Seasons MeSH
- Temperature MeSH
- Carbon * MeSH
- Publication type
- Journal Article MeSH
- Names of Substances
- Oxygen Isotopes MeSH
- Carbon * MeSH
Explaining species geographic distributions by macroclimate variables is the most common approach for getting mechanistic insights into large-scale diversity patterns and range shifts. However, species' traits influencing biophysical processes can produce a large decoupling from ambient air temperature, which can seriously undermine biogeographical inference. We combined stable oxygen isotope theory with a trait-based approach to assess leaf temperature during carbon assimilation (TL ) and its departure (ΔT) from daytime free air temperature during the growing season (Tgs ) for 158 plant species occurring from 3,400 to 6,150 m a.s.l. in Western Himalayas. We uncovered a general extent of temperature decoupling in the region. The interspecific variation in ΔT was best explained by the combination of plant height and δ13 C, and leaf dry matter content partly captured the variation in TL . The combination of TL and ΔT, with ΔT contributing most, explained the interspecific difference in elevational distributions. Stable oxygen isotope theory appears promising for investigating how plants perceive temperatures, a pivotal information to species biogeographic distributions.
College of Life Sciences and Oceanography Shenzhen University Shenzhen Guangdong Province China
Department of Botany Faculty of Science University of South Bohemia Ceske Budejovice Czech Republic
Faculty of Science University of South Bohemia Ceske Budejovice Czech Republic
Institute of Botany of the Czech Academy of Sciences Průhonice Czech Republic
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Ackerly, D. (2004). Functional strategies of chaparral shrubs in relation to seasonal water deficit and disturbance. Ecological Monographs, 74, 25-44. https://doi.org/10.1890/03-4022
Barbour, M. M., Schurr, U., Henry, B. K., Wong, S. C., & Farquahr, G. D. (2000). Variation in the oxygen isotope ratio of phloem sap sucrose from castor bean: Evidence in support of the Peclet effect. Plant Physiology, 123, 671-679. https://doi.org/10.1104/pp.123.2.671
Berry, J., & Bjorkman, O. (1980). Photosynthetic response and adaptation to temperature in higher plants. Annual Review of Plant Physiology, 31, 491-543. https://doi.org/10.1146/annurev.pp.31.060180.002423
Blum, A. (2005). Drought resistance, water-use efficiency, and yield potential - Are they compatible, dissonant, or mutually exclusive? Australian Journal of Agricultural Research, 56, 1159. https://doi.org/10.1071/ar05069
Bottinga, Y., & Craig, H. (1969). Oxygen isotope fractionation between CO2 and water, and the isotopic composition of marine atmospheric CO2. Earth and Planetary Science Letters, 5, 285-295. https://doi.org/10.1016/s0012-821x(68)80054-8
Bowen, G. J., & Revenaugh, J. (2003). Interpolating the isotopic composition of modern meteoric precipitation. Water Resources Research, 39, 1299. https://doi.org/10.1029/2003WR002086
Cernusak, L. A., Barbour, M. M., Arndt, S. K., Cheesman, A. W., English, N. B., Feild, T. S., … Farquhar, G. D. (2016). Stable isotopes in leaf water of terrestrial plants. Plant, Cell and Environment, 39, 1087-1102. https://doi.org/10.1111/pce.12703
Cernusak, L. A., Winter, K., & Turner, B. L. (2009). Physiological and isotopic (δ13C and δ18O) responses of three tropical tree species to water and nutrient availability. Plant, Cell and Environment, 32, 1441-1455. https://doi.org/10.1111/j.1365-3040.2009.02010.x
Dolezal, J., Dvorsky, M., Börner, A., Wild, J., & Schweingruber, F. H. (2018). Anatomy, age and ecology of high mountain plants in Ladakh, the Western Himalaya. Cham, Switzerland: Springer International Publishing.
Dolezal, J., Dvorsky, M., Kopecky, M., Liancourt, P., Hiiesalu, I., Macek, M., … Schweingruber, F. (2016). Vegetation dynamics at the upper elevational limit of vascular plants in Himalaya. Science Reports, 6. https://doi.org/10.1038/srep24881
Dong, N., Prentice, I. C., Harrison, S. P., Song, Q. H., & Zhang, Y. P. (2017). Biophysical homoeostasis of leaf temperature: A neglected process for vegetation and land-surface modelling. Global Ecology and Biogeography, 26(9), 998-1007. https://doi.org/10.1111/geb.12614
Dullinger, S., Gattringer, A., Thuiller, W., Moser, D., Zimmermann, N. E., Guisan, A., … Hülber, K. (2012). Extinction debt of high-mountain plants under twenty-first-century climate change. Nature Climate Change, 2, 619-622. https://doi.org/10.1038/nclimate1514
Dvorský, M., Altman, J., Kopecký, M., Chlumská, Z., Řeháková, K., Janatková, K., & Doležal, J. (2015). Vascular plants at extreme elevations in eastern Ladakh, northwest Himalayas. Plant Ecology and Diversity, 8, 571-584. https://doi.org/10.1080/17550874.2015.1018980
Dvorský, M., Doležal, J., de Bello, F., Klimešová, J., & Klimeš, L. (2011). Vegetation types of East Ladakh: Species and growth form composition along main environmental gradients. Applied Vegetation Science, 14, 132-147. https://doi.org/10.1111/j.1654-109X.2010.01103.x
Dvorský, M., Macek, M., Kopecký, M., Wild, J., & Doležal, J. (2017). Niche asymmetry of vascular plants increases with elevation. Journal of Biogeography, 44, 1418-1425. https://doi.org/10.1111/jbi.13001
Farquhar, G. D., Ehleringer, J. R., & Hubick, K. T. (1989). Carbon isotope discrimination and photosynthesis. Annual Review of Plant Physiology and Plant Molecular Biology, 40, 503-537. https://doi.org/10.1146/annurev.pp.40.060189.002443
Garnier, E., Navas, M.-L., & Grigulis, K. (2016). Plant functional diversity - organism traits, community structure, and ecosystem properties. Oxford, UK: Oxford University Press.
Gates, D. M. (1980). Biophysical ecology. New York, NY: Springer.
Givnish, T. J. (1987). Comparative studies of leaf form: Assessing the relative roles of selective pressures and phylogenetic constraints. New Phytologist, 106, 131-160. https://doi.org/10.1111/j.1469-8137.1987.tb04687.x
Grace, J. (1987). Climatic tolerance and the distribution of plants. New Phytologist, 106, 113-130. https://doi.org/10.1111/j.1469-8137.1987.tb04686.x
Grime, J. P. (1974). Vegetation classification by reference to strategies. Nature, 250, 26-31. https://doi.org/10.1038/250026a0
Guisan, A., & Zimmermann, N. E. (2000). Predictive habitat distribution models in ecology. Ecological Modelling, 135, 147-186. https://doi.org/10.1016/S0304-3800(00)00354-9
Harper, J. L. (1977). Population biology of plants. London, UK: Academic Press
Helliker, B. R., & Ehleringer, J. R. (2002). Differential 18O enrichment of leaf cellulose in C3 versus C4 grasses. Functional Plant Biology, 29, 435-442. https://doi.org/10.1071/pp01122
Helliker, B. R., & Richter, S. L. (2008). Subtropical to boreal convergence of tree-leaf temperatures. Nature, 454, 511-514. https://doi.org/10.1038/nature07031
Helliker, B. R., Song, X., Goulden, M. L., Clark, K., Bolstad, P., Munger, J. W., … Burns, S. P. (2018). Assessing the interplay between canopy energy balance and photosynthesis with cellulose δ18O: Large-scale patterns and independent ground-truthing. Oecologia, 187, 995-1007. https://doi.org/10.1007/s00442-018-4198-z
Holloway-Phillips, M., Cernusak, L. A., Barbour, M., Song, X., Cheesman, A., Munksgaard, N., … Farquhar, G. D. (2016). Leaf vein fraction influences the Péclet effect and 18O enrichment in leaf water. Plant, Cell and Environment, 39, 2414-2427. https://doi.org/10.1111/pce.12792
Kearney, M., & Porter, W. (2009). Mechanistic niche modelling: Combining physiological and spatial data to predict species' ranges. Ecology Letters, 12, 334-350. https://doi.org/10.1111/j.1461-0248.2008.01277.x
Keddy, P. A. (1992). Assembly and response rules: Two goals for predictive community ecology. Journal of Vegetation Science, 3, 157-164. https://doi.org/10.2307/3235676
Kobayashi, K., & Salam, M. U. (2000). Comparing simulated and measured values using mean squared deviation and its components. Agronomy Journal, 92, 345-352. https://doi.org/10.2134/agronj2000.922345x
Körner, C. (2001). One of nature's most innovative laboratories. Trends in Plant Science, 6, 7-8. https://doi.org/10.1016/S1360-1385(00)01832-X
Körner, C. (2003). Alpine plant life: Functional plant ecology of high mountain ecosystems (2nd ed.). Berlin; New York: Springer, Berlin.
Körner, C., & Hiltbrunner, E. (2018). The 90 ways to describe plant temperature. Perspectives in Plant Ecology, Evolution and Systematics, 30, 16-21. https://doi.org/10.1016/j.ppees.2017.04.004
Larcher, W. (2012). Bioclimatic temperatures in the high Alps. In C. Lütz (Ed.), Plants in Alpine regions (pp. 21-27). Vienna, Austria: Springer.
Le Bagousse-Pinguet, Y., Gross, N., Maestre, F. T., Maire, V., de Bello, F., Fonseca, C. R., … Liancourt, P. (2017). Testing the environmental filtering concept in global drylands. Journal of Ecology, 105, 1058-1069. https://doi.org/10.1111/1365-2745.12735
Liancourt, P., Boldgiv, B., Song, D. S., Spence, L. A., Helliker, B. R., Petraitis, P. S., & Casper, B. B. (2015). Leaf-trait plasticity and species vulnerability to climate change in a Mongolian steppe. Global Change Biology, 21, 3489-3498. https://doi.org/10.1111/gcb.12934
Liancourt, P., Le Bagousse-Pinguet, Y., Rixen, C., & Dolezal, J. (2017). SGH: Stress or strain gradient hypothesis? Insights from an elevation gradient on the roof of the world. Annals of Botany, 120, 29-38. https://doi.org/10.1093/aob/mcx037
Luo, Y., Dong, X., Yu, T., Shi, X., Li, Z., Yang, W., … Karrenberg, S. (2015). A single nucleotide deletion in gibberellin20-oxidase1 causes alpine dwarfism in arabidopsis. Plant Physiology, 168, 930-937. https://doi.org/10.1104/pp.15.00005
McGill, B. J. (2019). The what, how and why of doing macroecology. Global Ecology and Biogeography, 28, 6-17. https://doi.org/10.1111/geb.12855
Meng, T.-T., Wang, H., Harrison, S. P., Prentice, I. C., Ni, J., & Wang, G. (2015). Responses of leaf traits to climatic gradients: Adaptive variation versus compositional shifts. Biogeosciences, 12, 5339-5352. https://doi.org/10.5194/bg-12-5339-2015
Michaletz, S. T., Weiser, M. D., McDowell, N. G., Zhou, J., Kaspari, M., Helliker, B. R., & Enquist, B. J. (2016). The energetic and carbon economic origins of leaf thermoregulation. Nature Plants, 2, 16129. https://doi.org/10.1038/nplants.2016.129
Michaletz, S. T., Weiser, M. D., Zhou, J., Kaspari, M., Helliker, B. R., & Enquist, B. J. (2015). Plant thermoregulation: Energetics, trait-environment interactions, and carbon economics. Trends in Ecology & Evolution, 30, 714-724. https://doi.org/10.1016/j.tree.2015.09.006
Moles, A. T., Warton, D. I., Warman, L., Swenson, N. G., Laffan, S. W., Zanne, A. E., … Leishman, M. R. (2009). Global patterns in plant height. Journal of Ecology, 97, 923-932. https://doi.org/10.1111/j.1365-2745.2009.01526.x
Monroe, J. G., Markman, D. W., Beck, W. S., Felton, A. J., Vahsen, M. L., & Pressler, Y. (2018). Ecoevolutionary dynamics of carbon cycling in the anthropocene. Trends in Ecology & Evolution, 33, 213-225. https://doi.org/10.1016/j.tree.2017.12.006
Nicotra, A. B., Atkin, O. K., Bonser, S. P., Davidson, A. M., Finnegan, E. J., Mathesius, U., … van Kleunen, M. (2010). Plant phenotypic plasticity in a changing climate. Trends in Plant Science, 15, 684-692. https://doi.org/10.1016/j.tplants.2010.09.008
Noy-Meir, I. (1973). Desert ecosystems: Environment and producers. Annual Review of Ecology and Systematics, 4, 25-51. https://doi.org/10.1146/annurev.es.04.110173.000325
Pellissier, L., Bråthen, K. A., Vittoz, P., Yoccoz, N. G., Dubuis, A., Meier, E. S., … Guisan, A. (2013). Thermal niches are more conserved at cold than warm limits in arctic-alpine plant species. Global Ecology and Biogeography, 22, 933-941. https://doi.org/10.1111/geb.12057
Pérez-Harguindeguy, N., Díaz, S., Garnier, E., Lavorel, S., Poorter, H., Jaureguiberry, P., … Cornelissen, J. H. C. (2013). New handbook for standardised measurement of plant functional traits worldwide. Australian Journal of Botany, 61, 167. https://doi.org/10.1071/BT12225
Petraitis, P. S., Dunham, A. E., & Niewiarowski, P. H. (1996). Inferring multiple causality: The limitations of path analysis. Functional Ecology, 10, 421. https://doi.org/10.2307/2389934
Pollock, L. J., Morris, W. K., & Vesk, P. A. (2012). The role of functional traits in species distributions revealed through a hierarchical model. Ecography, 35, 716-725. https://doi.org/10.1111/j.1600-0587.2011.07085.x
Riddell, E. A., Odom, J. P., Damm, J. D., & Sears, M. W. (2018). Plasticity reveals hidden resistance to extinction under climate change in the global hotspot of salamander diversity. Science Advances, 4, eaar5471. https://doi.org/10.1126/sciadv.aar5471
Roche, P., Díaz-Burlinson, N., & Gachet, S. (2004). Congruency analysis of species ranking based on leaf traits: Which traits are the more reliable? Plant Ecology, 174, 37-48. https://doi.org/10.1023/B:VEGE.0000046056.94523.57
Roden, J. S., & Ehleringer, J. R. (1999). Hydrogen and oxygen isotope ratios of tree-ring cellulose for riparian trees grown long-term under hydroponically controlled environments. Oecologia, 121, 467-477. https://doi.org/10.1007/s004420050953
Roden, J. S., & Ehleringer, J. R. (2000). Hydrogen and oxygen isotope ratios of tree ring cellulose for field-grown riparian trees. Oecologia, 123, 481-489. https://doi.org/10.1007/s004420000349
Roden, J. S., Lin, G., & Ehleringer, J. R. (2000). A mechanistic model for interpretation of hydrogen and oxygen isotope ratios in tree-ring cellulose. Geochimica et Cosmochimica Acta, 64, 21-35. https://doi.org/10.1016/S0016-7037(99)00195-7
Roos, R. E., van Zuijlen, K., Birkemoe, T., Klanderud, K., Lang, S. I., Bokhorst, S., … Asplund, J. (2019). Contrasting drivers of community-level trait variation for vascular plants, lichens and bryophytes across an elevational gradient. Functional Ecology, 33, 2430-2446. https://doi.org/10.1111/1365-2435.13454
Salisbury, F. B., & Spomer, G. G. (1964). Leaf temperatures of alpine plants in the field. Planta, 60, 497-505. https://doi.org/10.1007/BF01894807
Scherrer, D., & Körner, C. (2010). Infra-red thermometry of alpine landscapes challenges climatic warming projections. Global Change Biology, 16, 2602-2613.
Shaver, G. R., Canadell, J., Chapin, F. S., Gurevitch, J., Harte, J., Henry, G., … Rustad, L. (2000). Global warming and terrestrial ecosystems: A conceptual framework for analysis. BioScience, 50, 871-882. https://doi.org/10.1641/0006-3568(2000)050[0871:GWATEA]2.0.CO;2
Song, X., Barbour, M. M., Saurer, M., & Helliker, B. R. (2011). Examining the large-scale convergence of photosynthesis-weighted tree leaf temperatures through stable oxygen isotope analysis of multiple data sets. New Phytologist, 192, 912-924. https://doi.org/10.1111/j.1469-8137.2011.03851.x
Song, X., Simonin, K. A., Loucos, K. E., & Barbour, M. M. (2015). Modelling non-steady-state isotope enrichment of leaf water in a gas-exchange cuvette environment. Plant, Cell & Environment, 38, 2618-2628. https://doi.org/10.1111/pce.12571
Stahl, U., Reu, B., & Wirth, C. (2014). Predicting species' range limits from functional traits for the tree flora of North America. Proceedings of the National Academy of Sciences of the United States of America, 111, 13739-13744. https://doi.org/10.1073/pnas.1300673111
Sternberg, L. (1989). Oxygen and hydrogen isotope ratios in plant cellulose: Mechanisms and applications. In P. W. Rundel, J. R. Ehleringer, & K. A. Nagy (Eds.), Stable isotopes in ecological research. Ecological Studies (Analysis and Synthesis) (Vol. 68). New York, NY: Springer.
Sternberg, L. (2009). Oxygen stable isotope ratios of tree-ring cellulose: The next phase of understanding. New Phytologist, 181, 553-562. https://doi.org/10.1111/j.1469-8137.2008.02661.x
Sternberg, L., & DeNiro, M. J. (1983). Isotopic composition of cellulose from C3, C4, and CAM plants growing near one another. Science, 220, 947-949. https://doi.org/10.1126/science.220.4600.947
Sternberg, L., DeNiro, M. J., & Savidge, R. A. (1986). Oxygen isotope exchange between metabolites and water during biochemical reactions leading to cellulose synthesis. Plant Physiology, 82, 423-427. https://doi.org/10.1104/pp.82.2.423
Thuiller, W., Lavorel, S., Araújo, M. B., Sykes, M. T., & Prentice, I. C. (2005). Climate change threats to plant diversity in Europe. Proceedings of the National Academy of Sciences of the United States of America, 102, 8245-8250. https://doi.org/10.1073/pnas.0409902102
West, J. B., Bowen, G. J., Cerling, T. E., & Ehleringer, J. R. (2006). Stable isotopes as one of nature’s ecological recorders. Trends in Ecology & Evolution, 21, 408-414. https://doi.org/10.1016/j.tree.2006.04.002
Wright, I. J., Reich, P. B., Westoby, M., Ackerly, D. D., Baruch, Z., Bongers, F., … Villar, R. (2004). The worldwide leaf economics spectrum. Nature, 428, 821-827. https://doi.org/10.1038/nature02403