Matthew HAWORTH, Angela GALLAGHER, Elysia SUM, Marlene HILL-DONNELLY

On the reconstruction of plant photosynthetic and stress physiology across the Triassic-Jurassic boundary

The Triassic-Jurassic boundary (TJB) coincides with major disruption to the carbon cycle and global warming as the Central Atlantic Magmatic Province developed. This resulted in both marine and terrestrial extinctions, with terrestrial plants thought to experience thermal stress as global temperatures and atmospheric CO2 levels rose. As plant compression fossils typically only preserve external morphological features, it has not been possible to reconstruct plant paleophysiology in order to elucidate the mechanisms underlying plant stress and extinction. Here we present a new approach allowing us to infer the photosynthetic performance and stress physiology of fossil plants, applied to fossil Ginkgoales across the TJB. We use correlations between the adaxial epidermal cell density of extant Ginkgo biloba and photosynthetic and protective stress physiology to infer the paleophysiological condition of Late Triassic-Early Jurassic-aged plants from Astartekløft, East Greenland. The density of fossil leaf adaxial epidermal cells indicates that photosynthetic performance of Ginkgoales became increasingly impaired towards the latter stages of the Triassic, before improving into the Early Jurassic. This is consistent with d13C isotope values, paleo-[CO2] levels, and global mean temperatures, suggesting that photosynthetic performance was influenced by the prevailing environmental conditions during the TJB event. Dissipation of absorbed energy as heat would also have risen towards the boundary as plant stress increased, in order to protect the photosynthetic physiology. The increase in dissipation of energy as heat, associated with a reduction in convective heat loss due to reduced transpiration rates, would have exacerbated plant thermal stress at the TJB, thus contributing to sudden biodiversity loss and ecological change.

Anahtar Kelimeler:

Key words: Triassic-Jurassic boundary, ginkgo, plant stress, thermal stress, paleophysiology, nonphotochemical quenching

On the reconstruction of plant photosynthetic and stress physiology across the Triassic-Jurassic boundary

Keywords:

Key words: Triassic-Jurassic boundary, ginkgo, plant stress, thermal stress, paleophysiology, nonphotochemical quenching,

PDF

___

Bacon KL, Belcher CM, Haworth M, McElwain JC (2013). Increased atmospheric SO 2 detected from changes in leaf physiognomy across the Triassic–Jurassic boundary interval of East Greenland. PLoS ONE 8: e60614.
Bacon KL, Belcher CM, Hesselbo SP, McElwain JC (2011). The Triassic-Jurassic boundary carbon-isotope excursions expressed in taxonomically identified leaf cuticles. Palaios 26: 461–469.
Bartiromo A, Guignard G, Lumaga MRB, Barattolo F, Chiodini G, Avino R, Guerriero G, Barale G (2012). Influence of volcanic gases on the epidermis of Pinus halepensis Mill. in Campi Flegrei, Southern Italy: a possible tool for detecting volcanism in present and past floras. J Volcanol Geotherm Res 233–234: 1–
Bartiromo A, Guignard G, Lumaga MRB, Barattolo F, Chiodini G, Avino R, Guerriero G, Barale G (2013). The cuticle micromorphology of in situ Erica arborea L. exposed to longterm volcanic gases. Environ Exp Bot 87: 197–206.
Beerling DJ, Berner RA (2002). Biogeochemical constraints on the Triassic-Jurassic boundary carbon cycle event. Global Biogeochem Cycles 16: 101–113.
Belcher CM, Mander L, Rein G, Jervis FX, Haworth M, Hesselbo SP, Glasspool IJ, McElwain JC (2010). Increased fire activity at the Triassic/Jurassic boundary in Greenland due to climate-driven floral change. Nat Geosci 3: 426–429.
Berner RA, Beerling DJ (2007). Volcanic degassing necessary to produce a CaCO 3 undersaturated ocean at the Triassic-Jurassic boundary. Palaeogeog Palaeoclimatol Palaeoecol 244: 368–373.
Bonis NR, Kürschner WM, Krystyn L (2009). A detailed palynological study of the Triassic-Jurassic transition in key sections of the Eiberg Basin (Northern Calcareous Alps, Austria). Rev Palaeobot Palynol 156: 376–400.
Cleveland DM, Nordt LC, Dworkin SI, Atchley SC (2008). Pedogenic carbonate isotopes as evidence for extreme climatic events preceding the Triassic-Jurassic boundary: implications for the biotic crisis? Geol Soc Am Bull 120: 1408–1415.
Dam G, Surlyk F (1992). Forced regressions in a large wave- and storm-dominated anoxic lake, Rhaetian-Sinemurian Kap Stewart Formation, East Greenland. Geology 20: 749–752.
Friend DJC, Pomeroy ME (1970). Changes in cell size and number associated with effects of light intensity and temperature on leaf morphology of wheat. Can J Bot 48: 85–90.
Galli MT, Jadoul F, Bernasconi SM, Weissert H (2005). Anomalies in global carbon cycling and extinction at the Triassic/Jurassic boundary: evidence from a marine C-isotope record. Palaeogeog
Palaeoclimatol Palaeoecol 216: 203–214. Gauslaa Y (1984). Heat resistance and energy budget in different
Scandinavian plants. Holarctic Ecology 7: 5–78. Grattan J, Sadler J (1999). Regional warming of the lower atmosphere in the wake of volcanic eruptions: the role of the Laki fissure eruption in the hot summer of 1783. In: Firth CR, McGuire WJ, editors. Volcanoes in the Quaternary. Volume 161. London, UK: Geological Society of London Special Publications, pp. 161–171.
Guex J, Bartolini A, Atudorei V, Taylor D (2004). High-resolution ammonite and carbon isotope stratigraphy across the TriassicJurassic boundary at New York Canyon (Nevada). Earth Planet Sci Lett 225: 29–41.
Hantemirov RM, Gorlanova LA, Shiyatov SG (2000). Pathological tree-ring structures in Siberian juniper (Juniperus sibirica Burgsd.) and their use for reconstructing extreme climatic events. Russian J Ecol 31: 185–192.
Harris TM (1937). The fossil flora of Scoresby Sound East Greenland, Part Stratigraphic relations of the plant beds. Meddelelser om Grİnland 112: 1–112.
Haworth M, Elliott-Kingston C, Gallagher A, Fitzgerald A, McElwain JC (2012). Sulphur dioxide fumigation effects on stomatal density and index of non-resistant plants: Implications for the stomatal palaeo-[CO 2
] proxy method. Rev Palaeobot Palynol 182: 44–54. Haworth M, McElwain J (2008). Hot, dry, wet, cold or toxic?
Revisiting the ecological significance of leaf and cuticular micromorphology. Palaeogeogr Palaeoclimatol Palaeoecol 262: 79– Hesselbo SP, Robinson SA, Surlyk F, Piasecki S (2002). 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.
Holroyd GH, Hetherington AM, Gray JE (2002). A role for the cuticular waxes in the environmental control of stomatal development. New Phytol 153: 433–439.
Hori RS, Fujiki T, Inoue E, Kimura JI (2007). Platinum group element anomalies and bioevents in the Triassic-Jurassic deep-sea sediments of Panthalassa. Palaeogeog Palaeoclimatol Palaeoecol 244: 391–406.
Horton P, Ruban A (2005). Molecular design of the photosystem II light-harvesting antenna: photosynthesis and photoprotection. J Exp Bot 56: 365–373.
Huynh TT, Poulsen CJ (2005). Rising atmospheric CO 2 as a possible trigger for the end-Triassic mass extinction. Palaeogeog Palaeoclimatol Palaeoecol 217: 223–242.
Kana R, Vass I (2008). Thermoimaging as a tool for studying lightinduced heating of leaves: correlation of heat dissipation with the efficiency of photosystem II photochemistry and nonphotochemical quenching. Environ Exp Bot 64: 90–96.
Kouwenberg LLR, Wagner R, Kürschner W, Visscher H (2005). Atmospheric CO 2 fluctuations during the last millennium reconstructed by stomatal frequency analysis of Tsuga heterophylla needles. Geology 33: 33–36.
Kürschner WM (1997). The anatomical diversity of recent and fossil leaves of the durmast oak (Quercus petraea Lieblein/Q. pseudocastanea Goeppert) - implications for their use as biosensors of palaeoatmospheric CO 2 levels. Rev Palaeobot Palynol 96: 1–30.
Kürschner WM, Bonis NR, Krystyn L (2007). Carbon-isotope stratigraphy and palynostratigraphy of the Triassic-Jurassic transition in the Tiefengraben section - Northern Calcareous Alps (Austria). Palaeogeog Palaeoclimatol Palaeoecol 244: 257– 2
Kürschner WM, Kvacek Z, Dilcher DL (2008). The impact of Miocene atmospheric carbon dioxide fluctuations on climate and the evolution of terrestrial ecosystems. Proc Nat Acad Sci USA 105: 449–453.
Mander L, Kürschner WM, McElwain JC (2013). Palynostratigraphy and vegetation history of the Triassic–Jurassic transition in East Greenland. J Geol Soc 170: 37–46.
Marzoli A, Bertrand H, Knight KB, Cirilli S, Buratti N, Verati C, Nomade S, Renne PR, Youbi N, Martini R et al (2004). Synchrony of the Central Atlantic magmatic province and the TriassicJurassic boundary climatic and biotic crisis. Geology 32: 973– 9
Maxwell K, Johnson GN (2000). Chlorophyll fluorescence - a practical guide. J Exp Bot 51: 659–668.
McElwain JC, Beerling DJ, Woodward FI (1999). Fossil plants and global warming at the Triassic-Jurassic boundary. Science 285: 1386–1390.
McElwain JC, Popa ME, Hesselbo SP, Haworth M, Surlyk F (2007). Macroecological responses of terrestrial vegetation to climatic and atmospheric change across the Triassic/Jurassic boundary in East Greenland. Paleobiology 33: 547–573.
Nicotra AB, Cosgrove MJ, Cowling A, Schlichting CD, Jones CS (2008). Leaf shape linked to photosynthetic rates and temperature optima in South African Pelargonium species. Oecologia 154: 625–635.
Palfy J, Demeny A, Haas J, Hetenyi M, Orchard MJ, Veto I (2001). Carbon isotope anomaly and other geochemical changes at the Triassic-Jurassic boundary from a marine section in Hungary. Geology 29: 1047–1050.
Pilkey WD (2002). Analysis and Design of Elastic Beams: Computational Methods. New York, NY, USA: John Wiley & Sons.
Poorter L, Bongers F (2006). Leaf traits are good predictors of plant performance across 53 rain forest species. Ecology 87: 1733– 17
Rahim MA, Fordham R (1991). Effect of shade on leaf and cell size and number of epidermal cells in garlic (Allium sativum). Ann Bot 67: 167–171.
Ruban AV, Berera R, Ilioaia C, van Stokkum IHM, Kennis JTM, Pascal AA, van Amerongen H, Robert B, Horton P, van Grondelle R (2007). Identification of a mechanism of photoprotective energy dissipation in higher plants. Nature 450: 575–578.
Ruhl M, Kürschner WM, Krystyn L (2009). Triassic-Jurassic organic carbon isotope stratigraphy of key sections in the western Tethys realm (Austria). Earth Planet Sci Lett 281: 169–187.
Schaller MF, Wright JD, Kent DV (2011). Atmospheric pCO 2 perturbations associated with the Central Atlantic Magmatic
Province. Science 331: 1404–1409.
Schoene B, Guex J, Bartolini A, Schaltegger U, Blackburn TJ (2010).
Correlating the end-Triassic mass extinction and flood basalt volcanism at the 100 ka level. Geology 38: 387–390. Seward AC (1892). Fossil Plants as Tests of Climate. London, UK: C. J. Clay Publishers.
Smith RY, Greenwood DR, Basinger JF (2010). Estimating paleoatmospheric pCO 2 during the Early Eocene Climatic
Optimum from stomatal frequency of Ginkgo, Okanagan Highlands, British Columbia, Canada. Palaeogeogr Palaeoclimatol Palaeoecol 293: 120–131. Sokal RR, Rohlf FJ (1995). Biometry: The Principles and Practices of
Statistics in Biological Research. 3rd ed. New York, NY, USA: Freeman and Company. Spicer RA (1980). The importance of depositional sorting to the biostratigraphy of plant megafossils. In: Dilcher DL, Taylor
TN, editors. Biostratigraphy of Fossil Plants: Successional and Paleoecological Analyses. Stroudsburg, PA, USA: Dowden, Hutchinson and Ross, Inc., pp. 171–183. Steinthorsdottir M, Jeram AJ, McElwain JC (2011). Extremely elevated CO 2 concentrations at the Triassic/Jurassic boundary. Palaeogeog
Palaeoclimatol Palaeoecol 308: 418–432. Sun BN, Dilcher DL, Beerling DJ, Zhang CJ, Yan DF, Kowalski E (2003).
Variation in Ginkgo biloba L. leaf characters across a climatic gradient in China. Proc Nat Acad Sci USA 100: 7141–7146.
Van de Schootbrugge B, Payne JL, Tomasovych A, Pross J, Fiebig J, Benbrahim M, Föllmi KB, Quan TM (2008). Carbon cycle perturbation and stabilization in the wake of the Triassic-Jurassic boundary mass-extinction event. Geochemistry Geophysics Geosystems 9: Q04028.
Van de Schootbrugge B, Quan TM, Lindström S, Püttmann W, Heunisch C, Pross J, Fiebig J, Petschick R, Röhling HG, Richoz S et al (2009). Floral changes across the Triassic/Jurassic boundary linked to flood basalt volcanism. Nat Geosci 2: 589–594.
Zielinski GA, Mayewski PA, Meeker LD, Whitlow S, Twickler MS, Morrison M, Meeses DA, Gow AJ, Alley RB (1994). Record of volcanism since 7000 B.C. from the GISP2 Greenland ice core and implications for the volcano-climate system. Science 264: 948–952.