Abstract
Climate change is likely to have altered the ecological functioning of past ecosystems, and is likely to alter functioning in the future; however, the magnitude and direction of such changes are difficult to predict. Here we use a deep-time case study to evaluate the impact of a well-constrained CO2-induced global warming event on the ecological functioning of dominant plant communities. We use leaf mass per area (LMA), a widely used trait in modern plant ecology, to infer the palaeoecological strategy of fossil plant taxa. We show that palaeo-LMA can be inferred from fossil leaf cuticles based on a tight relationship between LMA and cuticle thickness observed among extant gymnosperms. Application of this new palaeo-LMA proxy to fossil gymnosperms from East Greenland reveals significant shifts in the dominant ecological strategies of vegetation found across the Triassic–Jurassic transition. Late Triassic forests, dominated by low-LMA taxa with inferred high transpiration rates and short leaf lifespans, were replaced in the Early Jurassic by forests dominated by high-LMA taxa that were likely to have slower metabolic rates. We suggest that extreme CO2-induced global warming selected for taxa with high LMA associated with a stress-tolerant strategy and that adaptive plasticity in leaf functional traits such as LMA contributed to post-warming ecological success.
This is a preview of subscription content, access via your institution
Access options
Access Nature and 54 other Nature Portfolio journals
Get Nature+, our best-value online-access subscription
$29.99 / 30 days
cancel any time
Subscribe to this journal
Receive 12 digital issues and online access to articles
$119.00 per year
only $9.92 per issue
Buy this article
- Purchase on SpringerLink
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Grime, J. P. Benefits of plant diversity to ecosystems: immediate, filter and founder effects. J. Ecol. 86, 902–910 (1998).
Niinemets, Ü., Flexas, J. & Peñuelas, J. Evergreens favored by higher responsiveness to increased CO2 . Trends Ecol. Evol. 26, 136–142 (2011).
Ainsworth, E. A. & Long, S. P. What have we learned from 15 years of free-air CO2 enrichment (FACE)? A meta-analytic review of the responses of photosynthesis, canopy. New Phytol. 165, 351–371 (2005).
Steinthorsdottir, M., Jeram, A. J. & McElwain, J. C. Extremely elevated CO2 concentrations at the Triassic/Jurassic boundary. Palaeogeogr. Palaeoclimatol. Palaeoecol. 308, 418–432 (2011).
Bonis, N. R., Van Konijnenburg-Van Cittert, J. H. A. & Kürschner, W. M. Changing CO2 conditions during the end-Triassic inferred from stomatal frequency analysis on Lepidopteris ottonis (Goeppert) Schimper and Ginkgoites taeniatus (Braun) Harris. Palaeogeogr. Palaeoclimatol. Palaeoecol. 295, 146–161 (2010).
Schaller, M. F., Wright, J. D. & Kent, D. V. Atmospheric PCO2 perturbations associated with the central Atlantic magmatic province. Science 331, 1404 (2011).
McElwain, J. C., Beerling, D. J. & Woodward, F. I. Fossil plants and global warming at the Triassic-Jurassic boundary. Science 285, 1386–1390 (1999).
Wotzlaw, J.-F. et al. Towards accurate numerical calibration of the Late Triassic: high-precision U-Pb geochronology constraints on the duration of the Rhaetian. Geology 42, 571 (2014).
Lindström, S. et al. A new correlation of Triassic–Jurassic boundary successions in NW Europe, Nevada and Peru, and the Central Atlantic Magmatic Province: a time-line for the end-Triassic mass extinction. Palaeogeogr. Palaeoclimatol. Palaeoecol. 478, 80–102 (2017).
Mander, L., Kürschner, W. M. & McElwain, J. Palynostratigraphy and vegetation history of the Triassic–Jurassic transition in East Greenland. J. Geol. Soc. 170, 37–46 (2013).
Steinthorsdottir, M., Woodward, F. I., Surlyk, F. & McElwain, J. C. Deep-time evidence of a link between elevated CO2 concentrations and perturbations in the hydrological cycle via drop in plant transpiration. Geology 40, 815–818 (2012).
McElwain, J. C., Popa, M. E., Hesselbo, S. P., Haworth, D. M. & Surlyk, F. Macroecological responses of terrestrial vegetation to climatic and atmospheric change across the Triassic/Jurassic boundary in east Greenland. Paleobiology 33, 547–573 (2007).
Steinthorsdottir, M., Bacon, K. L., Popa, M. E., Bochner, L. & McElwain, J. C. Bennettitalean leaf cuticle fragments (here Anomozamites and Pterophyllum) can be used interchangeably in stomatal frequency-based palaeo-CO2 reconstructions. Palaeontology 54, 867–882 (2011).
Bacon, K. L., Belcher, C. M., Hesselbo, S. P. & McElwain, J. C. The Triassic-Jurassic boundary carbon-isotope excursions expressed in taxonomically identified leaf cuticles. Palaios 26, 461–469 (2011).
McElwain, J. C., Wagner, P. J. & Hesselbo, S. P. Fossil plant relative abundances indicate sudden loss of Late Triassic biodiversity in East Greenland. Science 324, 1554–1556 (2009).
Lindström, S. Palynofloral patterns of terrestrial ecosystem change during the end-Triassic event – a review. Geol. Mag. 153, 223–251 (2016).
Lindström, S. et al. Intense and widespread seismicity during the end-Triassic mass extinction due to emplacement of a large igneous province. Geology 43, 387 (2015).
Callegaro, S. et al. Microanalyses link sulfur from large igneous provinces and Mesozoic mass extinctions. Geology 42, 895 (2014).
Grime, J. P. Evidence for the existence of three primary strategies in plants and its relevance to ecological and evolutionary theory. Am. Nat. 111, 1169–1194 (1977).
Westoby, M., Falster, D. S., Moles, A. T., Vesk, P. A. & Wright, I. J. Plant ecological strategies: some leading dimensions of variation between species. Annu. Rev. Ecol. Syst. 33, 125–159 (2002).
Wright, I. J. et al. The worldwide leaf economics spectrum. Nature 428, 821–827 (2004).
Wright, I. J. & Westoby, M. Leaves at low versus high rainfall: coordination of structure, lifespan and physiology. New Phytol. 155, 403–416 (2002).
Reich, P. B., Walters, M. B. & Ellsworth, D. S. From tropics to tundra: global convergence in plant functioning. Proc. Natl Acad. Sci. USA 94, 13730–13734 (1997).
Riederer, M. in Annual Plant Reviews Biology of the Plant Cuticle Vol. 23 (eds Riederer, M. & Muller, C. ) 1–10 (Blackwell, 2006).
Onoda, Y., Richards, L. & Westoby, M. The importance of leaf cuticle for carbon economy and mechanical strength. New Phytol. 196, 441–447 (2012).
Royer, D. L. et al. Fossil leaf economics quantified: calibration, Eocene case study, and implications. Paleobiology 33, 574–589 (2007).
Royer, D. L., Miller, I. M., Peppe, D. J. & Hickey, L. J. Leaf economic traits from fossils support a weedy habit for early angiosperms. Am. J. Bot. 97, 438–445 (2010).
Haworth, M. & Raschi, A. An assessment of the use of epidermal micro-morphological features to estimate leaf economics of Late Triassic–Early Jurassic fossil Ginkgoales. Rev. Palaeobot. Palynol. 205, 1–8 (2014).
Moore, P., Van Miegroet, H. & Nicholas, N. Relative role of understory and overstory in carbon and nitrogen cycling in a southern Appalachian spruce–fir forest AES Publication 7863. Utah Agricultural Experiment Station, Utah State University, Logan, Utah. Can. J. For. Res. 37, 2689–2700 (2007).
Poorter, H., Niinemets, U., Poorter, L., Wright, I. J. & Villar, R. Causes and consequences of variation in leaf mass per area (LMA): a meta-analysis. New Phytol. 182, 565–588 (2009).
Huynh, T. & Poulsen, C. Rising atmospheric CO2 as a possible trigger for the end-Triassic mass extinction. Palaeogeogr. Palaeoclimatol. Palaeoecol. 217, 223–242 (2005).
Bacon, K. L., Haworth, M., Conroy, E. & McElwain, J. C. Can atmospheric composition influence plant fossil preservation potential via changes in leaf mass per area? A new hypothesis based on simulated palaeoatmosphere experiments. Palaeogeogr. Palaeoclimatol. Palaeoecol. 464, 51–64 (2016).
Berner, R. A. & Kothavala, Z. GEOCARB III: a revised model of atmospheric CO2 over Phanerozoic time. Science 301, 182–204 (2001).
Glasspool, I. J. & Scott, A. C. Phanerozoic concentrations of atmospheric oxygen reconstructed from sedimentary charcoal. Nat. Geosci. 3, 627–630 (2010).
van de Schootbrugge, B. et al. Floral changes across the Triassic/Jurassic boundary linked to flood basalt volcanism. Nat. Geosci. 2, 589–594 (2009).
Bacon, K. L., Belcher, C. M., Haworth, M. & McElwain, J. C. Increased atmospheric SO2 detected from changes in leaf physiognomy across the Triassic–Jurassic boundary interval of East Greenland. PLoS ONE 8, e60614 (2013).
Bacon, K. L. Tracking and Interpreting Leaf Physiognomy and Stable Carbon Isotopic Composition across the Triassic-Jurassic Boundary PhD thesis, Univ. College Dublin (2012).
Garsed, S. G., Farrar, J. F. & Rutter, A. J. The effects of low concentrations of sulphur dioxide on the growth of four broadleaved tree species. J. Appl. Ecol. 16, 217–226 (1979).
Temple, P. J., Fa, C. H. & Taylor, O. C. Effects of SO2 on stomatal conductance and growth of Phaseolus vulgaris. Environ. Pollut. A Ecol. Biol. 37, 267–279 (1985).
Whitmore, M. E. & Mansfield, T. A. Effects of long-term exposures to SO2 and NO2 on Poa pratensis and other grasses. Environ. Pollut. A Ecol. Biol. 31, 217–235 (1983).
Jones, T. & Mansfield, T. A. The effect of SO2 on growth and development of seedlings of Phleum pratense under different light and temperature environments. Environ. Pollut. A Ecol. Biol. 27, 57–71 (1982).
Bell, J. N. B., Rutter, A. J. & Relton, J. Studies on the effects of low levels of sulphur dioxide on the growth of Lolium perenne L. New Phytol. 83, 627–643 (1979).
Nicotra, A. B. et al. Plant phenotypic plasticity in a changing climate. Trends Plant Sci. 15, 684–692 (2010).
Ghalambor, C. K., McKay, J. K., Carroll, S. P. & Reznick, D. N. Adaptive versus non-adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments. Funct. Ecol. 21, 394–407 (2007).
Del Tredici, P. et al. The Ginkgos of Tian Mu Shan. Conserv. Biol. 6, 202–209 (1992).
Royer, D. L., Hickey, L. J. & Wing, S. L. Ecological conservatism in the “living fossil” Ginkgo. Paleobiology 29, 84–104 (2003).
Currano, E. D. et al. Sharply increased insect herbivory during the Paleocene–Eocene Thermal Maximum. Proc. Natl. Acad. Sci. USA 105, 1960–1964 (2008).
Blonder, B., Royer, D. L., Johnson, K. R., Miller, I. & Enquist, B. J. Plant ecological strategies shift across the Cretaceous–paleogene boundary. PLoS Biol. 12, e1001949 (2014).
Cornwell, W. K., Godoy, Ó. & Westoby, M. The leaf economic spectrum drives litter decomposition within regional floras worldwide. Ecol. Lett. 1071, 1065–1071 (2008).
Bonis, N. R. & Kürschner, W. M. Vegetation history, diversity patterns, and climate change across the Triassic/Jurassic boundary. Paleobiology 38, 240–264 (2012).
McElwain, J. C., Yiotis, C. & Lawson, T. Using modern plant trait relationships between observed and theoretical maximum stomatal conductance and vein density to examine patterns of plant macroevolution. New Phytol. 209, 94–103 (2015).
Utescher, T. & Mosbrugger, V. Eocene vegetation patterns reconstructed from plant diversity—a global perspective. Palaeogeogr. Palaeoclimatol. Palaeoecol. 247, 243–271 (2007).
Spicer, R. A. The formation and interpretation of plant fossil assemblages. Adv. Bot. Res. Inc. Adv Plant Pathol. 16, 95–191 (1989).
Schneider, C. A., Rasband, W. S. & Eliceiri, K. W. NIH image to imageJ 25 years of image analysis. Nat. Methods 9, 671–675 (2012).
Dykstra, M. J. A Manual of Applied Techniques for biological electron microscopy (Plenum Press, 1993).
Plummer, M. Proceedings of the 3rd International Workshop on Distributed Statistical Computing (DSC, 2003).
R Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2012); http://www.R-project.org
Plummer, M. rjags: Bayesian Graphical Models using MCMC. (CRAN, 2016); http://CRAN.R-project.org/package=rjags
Gelman, A. & Hill, J. Data analysis using regression and multi-level/hierarchical models 625 (Cambridge Univ. Press, 2007).
Parnell, A. C., Haslett, J., Allen, J. R. M., Buck, C. E. & Huntley, B. A flexible approach to assessing synchroneity of past events using Bayesian reconstructions of sedimentation history. Quat. Sci. Rev. 27, 1872–1885 (2008).
Webb, C. O. & Donoghue, M. J. Phylomatic: tree assembly for applied phylogenetics. Mol. Ecol. Notes 5, 181–183 (2005).
Webb, C. O., Ackerly, D. D. & Kembel, S. W. Phylocom: software for the analysis of phylogenetic community structure and trait evolution. Bioinformatics 24, 2098–2100 (2008).
Christianson, M. L. & Niklas, K. J. Patterns of diversity in leaves from canopies of Ginkgo biloba are revealed using Specific Leaf Area as a morphological character. Am. J. Bot. 98, 1068–1076 (2011).
Hesselbo, S. P., Robinson, S. A., Surlyk, F. & Piasecki, S. Terrestrial and marine extinction at the Triassic–Jurassic boundary synchronized with major carbon-cycle perturbation: a link to initiation of massive volcanism? Geology 30, 251–254 (2002).
Acknowledgements
We are grateful to D. Birch and N. Vella for microscopy assistance at Macquarie University Microscopy Unit. We also thank staff at the Sydney Royal Botanic Gardens (F. Jackson, D. Bidwell and P. Nicolson) and National Botanic Gardens, Ireland (M. Jebb and C. Kelleher) for permission to sample leaf material. K. Ziemińska and T. Tosens helped with queries on plant anatomy. We thank D. Royer and S. Lindström for their comments. We thank L. Furlong for the graphics and J. Elkink for statistical advice. This research is funded by Science Foundation Ireland PI grant (11/P1/1103) (J.C.M., W.K.S., K.L.B, I.J.W.), University College Dublin (SF1036) (W.K.S.), Royal Irish Academy (W.K.S.), Australian Research Council (FT100100910) (I.J.W.) and Macquarie University (I.J.W., T.I.L.).
Author information
Authors and Affiliations
Contributions
W.K.S., I.J.W. and J.C.M. designed the study, interpreted the data and wrote the paper with feedback from all authors; W.K.S. and A.C.P. performed the statistical analyses; W.K.S. and T.I.L. conducted the microscopy work; W.K.S. contributed to the cell-LMA proxy data; K.L.B. contributed to the paleoatmosphere experiment and petiole-LMA proxy results; M.S. contributed to the macrofossil morphotype and herbivory data.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing financial interests.
Supplementary information
Supplementary Information
Supplementary Text, Supplementary Tables 1–13, Supplementary Figs 1–10, Supplementary References. (PDF 1686 kb)
Supplementary Data
Palaeo LMA proxy data. Dataset 1: cuticle LMA proxy training. Dataset 2: cuticle LMA proxy fossil. Dataset 3: epidermal LMA proxy fossil. Dataset 4: petiole LMA proxy fossil. (XLSX 46 kb)
Rights and permissions
About this article
Cite this article
Soh, W., Wright, I., Bacon, K. et al. Palaeo leaf economics reveal a shift in ecosystem function associated with the end-Triassic mass extinction event. Nature Plants 3, 17104 (2017). https://doi.org/10.1038/nplants.2017.104
Received:
Accepted:
Published:
DOI: https://doi.org/10.1038/nplants.2017.104