Skip to main content

Thank you for visiting You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Palaeo leaf economics reveal a shift in ecosystem function associated with the end-Triassic mass extinction event

A Corrigendum to this article was published on 31 July 2017


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.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.


All prices are NET prices.

Figure 1: Palaeo-LMA proxy development.
Figure 2: LMA of fossil plant species from Astartekløft in East Greenland, pooled by plant groups and plant beds.
Figure 3: Ecological traits of Bennettitales and Ginkgoales plotted against the Tr–J geologic time scale, indicated by the plant sporomorph zonation10 and global warming period.


  1. 1

    Grime, J. P. Benefits of plant diversity to ecosystems: immediate, filter and founder effects. J. Ecol. 86, 902–910 (1998).

    Article  Google Scholar 

  2. 2

    Niinemets, Ü., Flexas, J. & Peñuelas, J. Evergreens favored by higher responsiveness to increased CO2 . Trends Ecol. Evol. 26, 136–142 (2011).

    Article  Google Scholar 

  3. 3

    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).

    Article  Google Scholar 

  4. 4

    Steinthorsdottir, M., Jeram, A. J. & McElwain, J. C. Extremely elevated CO2 concentrations at the Triassic/Jurassic boundary. Palaeogeogr. Palaeoclimatol. Palaeoecol. 308, 418–432 (2011).

    Article  Google Scholar 

  5. 5

    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).

    Article  Google Scholar 

  6. 6

    Schaller, M. F., Wright, J. D. & Kent, D. V. Atmospheric PCO2 perturbations associated with the central Atlantic magmatic province. Science 331, 1404 (2011).

    CAS  Article  Google Scholar 

  7. 7

    McElwain, J. C., Beerling, D. J. & Woodward, F. I. Fossil plants and global warming at the Triassic-Jurassic boundary. Science 285, 1386–1390 (1999).

    CAS  Article  Google Scholar 

  8. 8

    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).

    CAS  Article  Google Scholar 

  9. 9

    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).

    Article  Google Scholar 

  10. 10

    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).

    Article  Google Scholar 

  11. 11

    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).

    Article  Google Scholar 

  12. 12

    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).

    Article  Google Scholar 

  13. 13

    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).

    Article  Google Scholar 

  14. 14

    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).

    Article  Google Scholar 

  15. 15

    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).

    CAS  Article  Google Scholar 

  16. 16

    Lindström, S. Palynofloral patterns of terrestrial ecosystem change during the end-Triassic event – a review. Geol. Mag. 153, 223–251 (2016).

    Article  Google Scholar 

  17. 17

    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).

    Article  Google Scholar 

  18. 18

    Callegaro, S. et al. Microanalyses link sulfur from large igneous provinces and Mesozoic mass extinctions. Geology 42, 895 (2014).

    CAS  Article  Google Scholar 

  19. 19

    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).

    Article  Google Scholar 

  20. 20

    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).

    Article  Google Scholar 

  21. 21

    Wright, I. J. et al. The worldwide leaf economics spectrum. Nature 428, 821–827 (2004).

    CAS  Article  Google Scholar 

  22. 22

    Wright, I. J. & Westoby, M. Leaves at low versus high rainfall: coordination of structure, lifespan and physiology. New Phytol. 155, 403–416 (2002).

    Article  Google Scholar 

  23. 23

    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).

    CAS  Article  Google Scholar 

  24. 24

    Riederer, M. in Annual Plant Reviews Biology of the Plant Cuticle Vol. 23 (eds Riederer, M. & Muller, C. ) 1–10 (Blackwell, 2006).

    Google Scholar 

  25. 25

    Onoda, Y., Richards, L. & Westoby, M. The importance of leaf cuticle for carbon economy and mechanical strength. New Phytol. 196, 441–447 (2012).

    Article  Google Scholar 

  26. 26

    Royer, D. L. et al. Fossil leaf economics quantified: calibration, Eocene case study, and implications. Paleobiology 33, 574–589 (2007).

    Article  Google Scholar 

  27. 27

    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).

    Article  Google Scholar 

  28. 28

    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).

    Article  Google Scholar 

  29. 29

    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).

    CAS  Article  Google Scholar 

  30. 30

    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).

    Article  Google Scholar 

  31. 31

    Huynh, T. & Poulsen, C. Rising atmospheric CO2 as a possible trigger for the end-Triassic mass extinction. Palaeogeogr. Palaeoclimatol. Palaeoecol. 217, 223–242 (2005).

    Article  Google Scholar 

  32. 32

    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).

    Article  Google Scholar 

  33. 33

    Berner, R. A. & Kothavala, Z. GEOCARB III: a revised model of atmospheric CO2 over Phanerozoic time. Science 301, 182–204 (2001).

    CAS  Google Scholar 

  34. 34

    Glasspool, I. J. & Scott, A. C. Phanerozoic concentrations of atmospheric oxygen reconstructed from sedimentary charcoal. Nat. Geosci. 3, 627–630 (2010).

    CAS  Article  Google Scholar 

  35. 35

    van de Schootbrugge, B. et al. Floral changes across the Triassic/Jurassic boundary linked to flood basalt volcanism. Nat. Geosci. 2, 589–594 (2009).

    CAS  Article  Google Scholar 

  36. 36

    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).

    CAS  Article  Google Scholar 

  37. 37

    Bacon, K. L. Tracking and Interpreting Leaf Physiognomy and Stable Carbon Isotopic Composition across the Triassic-Jurassic Boundary PhD thesis, Univ. College Dublin (2012).

  38. 38

    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).

    CAS  Article  Google Scholar 

  39. 39

    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).

    CAS  Article  Google Scholar 

  40. 40

    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).

    CAS  Article  Google Scholar 

  41. 41

    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).

    CAS  Article  Google Scholar 

  42. 42

    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).

    CAS  Article  Google Scholar 

  43. 43

    Nicotra, A. B. et al. Plant phenotypic plasticity in a changing climate. Trends Plant Sci. 15, 684–692 (2010).

    CAS  Article  Google Scholar 

  44. 44

    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).

    Article  Google Scholar 

  45. 45

    Del Tredici, P. et al. The Ginkgos of Tian Mu Shan. Conserv. Biol. 6, 202–209 (1992).

    Article  Google Scholar 

  46. 46

    Royer, D. L., Hickey, L. J. & Wing, S. L. Ecological conservatism in the “living fossil” Ginkgo. Paleobiology 29, 84–104 (2003).

    Article  Google Scholar 

  47. 47

    Currano, E. D. et al. Sharply increased insect herbivory during the Paleocene–Eocene Thermal Maximum. Proc. Natl. Acad. Sci. USA 105, 1960–1964 (2008).

    CAS  Article  Google Scholar 

  48. 48

    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).

    Article  Google Scholar 

  49. 49

    Cornwell, W. K., Godoy, Ó. & Westoby, M. The leaf economic spectrum drives litter decomposition within regional floras worldwide. Ecol. Lett. 1071, 1065–1071 (2008).

    Article  Google Scholar 

  50. 50

    Bonis, N. R. & Kürschner, W. M. Vegetation history, diversity patterns, and climate change across the Triassic/Jurassic boundary. Paleobiology 38, 240–264 (2012).

    Article  Google Scholar 

  51. 51

    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).

    Article  Google Scholar 

  52. 52

    Utescher, T. & Mosbrugger, V. Eocene vegetation patterns reconstructed from plant diversity—a global perspective. Palaeogeogr. Palaeoclimatol. Palaeoecol. 247, 243–271 (2007).

    Article  Google Scholar 

  53. 53

    Spicer, R. A. The formation and interpretation of plant fossil assemblages. Adv. Bot. Res. Inc. Adv Plant Pathol. 16, 95–191 (1989).

    Google Scholar 

  54. 54

    Schneider, C. A., Rasband, W. S. & Eliceiri, K. W. NIH image to imageJ 25 years of image analysis. Nat. Methods 9, 671–675 (2012).

    CAS  Article  Google Scholar 

  55. 55

    Dykstra, M. J. A Manual of Applied Techniques for biological electron microscopy (Plenum Press, 1993).

    Book  Google Scholar 

  56. 56

    Plummer, M. Proceedings of the 3rd International Workshop on Distributed Statistical Computing (DSC, 2003).

    Google Scholar 

  57. 57

    R Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2012);

  58. 58

    Plummer, M. rjags: Bayesian Graphical Models using MCMC. (CRAN, 2016);

  59. 59

    Gelman, A. & Hill, J. Data analysis using regression and multi-level/hierarchical models 625 (Cambridge Univ. Press, 2007).

    Google Scholar 

  60. 60

    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).

    Article  Google Scholar 

  61. 61

    Webb, C. O. & Donoghue, M. J. Phylomatic: tree assembly for applied phylogenetics. Mol. Ecol. Notes 5, 181–183 (2005).

    Article  Google Scholar 

  62. 62

    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).

    CAS  Article  Google Scholar 

  63. 63

    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).

    Article  Google Scholar 

  64. 64

    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).

    Article  Google Scholar 

Download references


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




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

Correspondence to W. K. Soh.

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

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

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).

Download citation

Further reading


Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing