Hostname: page-component-669899f699-tpknm Total loading time: 0 Render date: 2025-04-29T05:08:45.502Z Has data issue: false hasContentIssue false
  • English
  • Français

Fossil evidence for low gas exchange capacities for Early Cretaceous angiosperm leaves

Published online by Cambridge University Press:  08 April 2016

Taylor S. Feild ,
Garland R. Upchurch Jr. ,
David S. Chatelet ,
Timothy J. Brodribb ,
Kunsiri C. Grubbs ,
Marie-Stéphanie Samain  and
Stefan Wanke
Taylor S. Feild*
Affiliation:
School of Biological Sciences, Monash University, Clayton Campus, Australia. E-mail: [email protected]
Garland R. Upchurch Jr.
Affiliation:
Department of Ecology and Evolutionary Biology, University of Tennessee, Knoxville, Tennessee 37996
David S. Chatelet
Affiliation:
Department of Plant Science, University of Tasmania, Hobart, Tasmania, Australia
Timothy J. Brodribb
Affiliation:
Department of Biology, Texas State University, San Marcos, Texas
Kunsiri C. Grubbs
Affiliation:
Department of Biology, Winthrop University, Rock Hill, South Carolina
Marie-Stéphanie Samain
Affiliation:
Ghent University, Department of Biology, Research Group Spermatophytes, B-9000 Ghent, Belgium
Stefan Wanke
Affiliation:
Technische Universität Dresden, Institut fur Botanik, 01062 Dresden, Germany
*
∗Corresponding author
Get access Rights & Permissions [Opens in a new window]

Abstract

The photosynthetic gas exchange capacities of early angiosperms remain enigmatic. Nevertheless, many hypotheses about the causes of early angiosperm success and how angiosperms influenced Mesozoic ecosystem function hinge on understanding the maximum capacity for early angiosperm metabolism. We applied structure-functional analyses of leaf veins and stomatal pore geometry to determine the hydraulic and diffusive gas exchange capacities of Early Cretaceous fossil leaves. All of the late Aptian—early Albian angiosperms measured possessed low vein density and low maximal stomatal pore area, indicating low leaf gas exchange capacities in comparison to modern ecologically dominant angiosperms. Gas exchange capacities for Early Cretaceous angiosperms were equivalent or lower than ferns and gymnosperms. Fossil leaf taxa from Aptian to Paleocene sediments previously identified as putative stem-lineages to Austrobaileyales and Chloranthales had the same gas exchange capacities and possibly leaf water relations of their living relatives. Our results provide fossil evidence for the hypothesis that high leaf gas exchange capacity is a derived feature of later angiosperm evolution. In addition, the leaf gas exchange functions of austrobaileyoid and chloranthoid fossils support the hypothesis that comparative research on the biology of living basal angiosperm lineages reveals genuine signals of Early Cretaceous angiosperm ecophysiology.

Type
Articles
Information
Paleobiology , Volume 37 , Issue 2 , Spring 2011 , pp. 195 - 213
Copyright
Copyright © The Paleontological Society 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Article purchase

Temporarily unavailable

References

Literature Cited

Ackerly, D. D., and Donoghue, M. J. 1998. Leaf size, sapling allometry and Corner's rules: a phylogenetic study of correlated evolution in maples (Acer). American Naturalist 152:767–791.Google Scholar
Archangelsky, S., Barreda, V., Passalia, M. G., Gandolfo, M. A., Pramparo, M., Romero, E., Cuneo, R., Zamuner, A., Iglesias, A., Llorens, M., Puebla, G. G., Quattrocchio, M., and Volkheimer, W. 2009. Early angiosperm diversification: evidence from southern South America. Cretaceous Research 30:1073–1082.CrossRefGoogle Scholar
Barclay, R. S., McElwain, J. C., and Sageman, B. B. 2010. Volcanic CO2 pulse activates carbon sequestration during Oceanic Anoxic Event 2. Nature Geoscience 3:205–208.CrossRefGoogle Scholar
Blackman, C. J., Brodribb, T. J., and Jordan, G. J. 2010. Leaf hydraulic vulnerability is related to conduit dimensions and drought resistance across a diverse range of woody angiosperms. New Phytologist 188:doi: 10.1111/j.1469–8137.2010.03439.x Google Scholar
Bond, W. J. 1989. The tortoise and the hare—ecology of angiosperm dominance and gymnosperm persistence. Biological Journal of the Linnean Society 36:227–249.CrossRefGoogle Scholar
Bond, W. J., and Scott, A. C. 2010. Fire and the spread of flowering plants in the Cretaceous. New Phytologist 188:doi: 10.1111/j.1469–8137.2010.03418.x CrossRefGoogle ScholarPubMed
Boyce, C. K., Brodribb, T. J., Feild, T. S., and Zwieniecki, M. A. 2009. Angiosperm leaf vein evolution was physiologically and environmentally transformative. Proceedings of the Royal Society of London B 276:1771–1776.Google Scholar
Brenner, G. J. 1996. Evidence for the earliest stage of angiosperm pollen evolution: a paleoequatorial section from Israel. Pp. 91–115 in Taylor, D. W. and Hickey, L. J., eds. Flowering plant origin, evolution, and phylogeny. Chapman and Hall, New York.CrossRefGoogle Scholar
Brodribb, T., and Feild, T. S. 2000. Stem hydraulic supply is linked to leaf photosynthetic capacity: evidence from New Caledonian and Tasmanian rainforests. Plant, Cell and Environment 23:1381–1388.Google Scholar
Brodribb, T., and Feild, T. S. 2008. The evolutionary significance of flat-leaves in the conifer, Pinus krempfii in Vietnamese rainforest. New Phytologist 178:201–209.Google Scholar
Brodribb, T., and Feild, T. S. 2010. Leaf hydraulic evolution led to a surge in leaf photosynthetic capacity during early angiosperm diversification. Ecology Letters 13:175–183.Google Scholar
Brodribb, T. J., and Hill, R. S. 1997. Imbricacy and stomatal wax plugs reduce maximum leaf conductance in Southern Hemisphere conifers. Australian Journal of Botany 45:657–668.Google Scholar
Brodribb, T. J., Feild, T. S., and Jordan, G. J. 2007. Leaf maximum photosynthetic rate and venation are linked by hydraulics. Plant Physiology 144:1890–1898.Google Scholar
Carpenter, K. J. 2005. Stomatal architecture and evolution in basal angiosperms. American Journal of Botany 92:1595–1615.Google Scholar
Coiffard, C., Gomez, B., and Thevenard, F. 2007. Early Cretaceous angiosperm invasion of western Europe and major environmental changes. Annals of Botany 100:545–553.CrossRefGoogle ScholarPubMed
Cuneo, R., and Gandolfo, M. A. 2005. Angiosperm leaves from the Kachaike Formation, Lower Cretaceous of Patagonia, Argentina. Review of Paleobotany and Palynology 136:29–47.Google Scholar
Doyle, J. A. 1999. The rise of angiosperms as seen in the African Cretaceous pollen record. Pp. 3–29 in Scott, L., Cadman, A. and Verhoeven, R., eds. Palaeoecology of Africa and the surrounding islands, Vol. 26. A. A. Balkema, Rotterdam.Google Scholar
Doyle, J. A. 2007. Systematic value of leaf architecture across the angiosperms in light of molecular phylogenetic analyses. Courier Forschungsinstitut Senckenberg 258:21–37.Google Scholar
Doyle, J. A., and Hickey, L. J. 1976. Pollen and leaves from the mid-Cretaceous Potomac Group and their bearing on early angiosperm evolution. Pp. 139–206 in Beck, C. B., ed. Origin and early evolution of angiosperms. Columbia University Press, New York.Google Scholar
Endress, P. K., and Doyle, J. A. 2009. Reconstruction the ancestral angiosperm flower and its initial specializations. American Journal of Botany 96:22–66.Google Scholar
Feild, T. S. 2009. Regeneration ecology of early angiosperm seeds and seedlings: integrating inferences from extant basal lineages and fossils. Pp. 130–149 in Leck, M. A., Parker, V. T., Simpson, R. L., eds. Seedling ecology and evolution. Cambridge University Press.Google Scholar
Feild, T. S., and Arens, N. C. 2007. The ecophysiology of early angiosperms. Plant, Cell and Environment 30:291–309.Google Scholar
Feild, T. S., and Balun, L. 2008. Xylem hydraulic and photosynthetic function of Gnetum (Gnetales) species from Papua New Guinea. New Phytologist 177:665–675.Google Scholar
Feild, T. S., Arens, N. C., Doyle, J. A., Dawson, T. E., and Donoghue, M. J. 2004. Dark and disturbed: a new image of early angiosperm ecology. Paleobiology 30:82–107.Google Scholar
Feild, T. S., Sage, T. L., Czerniak, C., and Illes, W. J. D. 2005. Hydathodal leaf teeth of Chloranthus japonicus prevent guttation-induced flooding of the mesophyll. Plant, Cell, and Environment 28:1179–1190.Google Scholar
Feild, T. S., Chatelet, D. S., and Brodribb, T. J. 2009. Ancestral xerophobia: a hypothesis on the whole plant ecophysiology of early angiosperms. Geobiology 7:237–264.Google Scholar
Fletcher, B. J., Brentnall, S. J., Anderson, C. W., Berner, R. A., and Beerling, D. J. 2008. Atmospheric carbon dioxide linked with Mesozoic and early Cenozoic climate change. Nature Geoscience 1:43–48.Google Scholar
Franks, P. J., and Beerling, D. J. 2009. Maximum leaf conductance driven by CO2 effects on stomatal size and density over geologic time. Proceedings of the National Academy of Sciences USA 106:10343–10347.Google Scholar
Franks, P. J., and Farquhar, G. D. 2007. The mechanical diversity of stomata and its significance in gas-exchange control. Plant Physiology 143:78–87.Google Scholar
Fuller, D. Q., and Hickey, L. J. 2005. Systematics and leaf architecture of the Gunneraceae. Botanical Review 71:295–353.Google Scholar
Gastaldo, R. A., Douglass, D. P., and McCarroll, S. M. 1987. Origin, characteristics, and provenance of plant macrodetritus in a Holocene crevasse splay, Mobile Delta, Alabama. Palaios 2:229–240.CrossRefGoogle Scholar
Glasspool, I. J., and Scott, A. C. 2010. Phanerozoic concentrations of atmospheric oxygen reconstructed from sedimentary charcoal. Nature Geoscience (in press).CrossRefGoogle Scholar
Heimhofer, U., Hochuli, P., Burla, S., Dinis, J., and Weissert, H. 2005. Timing of Early Cretaceous angiosperm diversification and possible links to major paleoenvironmental change. Geology 33:141–144.Google Scholar
Hickey, L. J., and Doyle, J. A. 1977. Early Cretaceous fossil evidence for angiosperm evolution. Botanical Review 43:3–104.CrossRefGoogle Scholar
Hudson, P. J., Razanatsoa, J., and Feild, T. S. 2010. Early vessel evolution and the diversification of wood function: insights from Malagasy Canellales. American Journal of Botany 97:80–93.Google Scholar
Ito, H., Ito, S., Matsui, T., and Marutani, T. 2006. Effect of fluvial and geomorphic disturbances on habitat segregation of tree species in a sedimentation-dominated riparian forest in warm-temperate mountainous region in southern Japan. Journal of Forest Research 11:405–417.Google Scholar
Jansen, R. K., Cai, Z., Raubeson, L. A., Daniell, H., dePamphilis, C. W., Leebens-Mack, J., Muller, K. F., Guisinger-Bellian, M., Haberle, R. C., Hansen, A. K., Chumley, T. W., Lee, S. B., Peery, R., McNeal, J. R., Kuehl, J. V., and Boore, J. L. 2007. Analysis of 81 genes from 64 plastid genomes resolves relationships in angiosperms and identifies genome-scale evolutionary patterns. Proceedings of the National Academy of Sciences USA 104:19369–19374.Google Scholar
Jones, H. J. 1993. Plants and microclimates. Cambridge University Press, Cambridge.Google Scholar
Kaiser, H. 2009. The relation between stomatal aperture and gas exchange under consideration of pore geometry and diffusional resistance in the mesophyll. Plant, Cell and Environment 32:1091–1098.Google Scholar
Keeling, H. C., Phillips, O. L. 2007. A calibration method for the crown illumination index for assessing forest light environments. Forest Ecology and Management 242:431–437.Google Scholar
Kerstiens, G. 1998. Shade-tolerance as a predictor of responses to elevated CO2 in trees. Physiologia Plantarum 102:472–480.Google Scholar
Körner, C. 1995. Leaf diffusive conductances in the major vegetation types of the globe. Pp. 463–490 in Schulze, E.-D. and Caldwell, M. M., eds. Ecophysiology of photosynthesis. Springer, Berlin.Google Scholar
Körner, C. 2009. Responses of humid tropical trees to rising CO2 . Annual Review of Ecology and Systematics 40:61–79.Google Scholar
Lawson, T., James, W., and Weyers, J. 1998. A surrogate measure of stomatal aperture. Journal of Experimental Botany 325:1397–1403.Google Scholar
Lupia, R., Lidgard, S.S., and Crane, P. R. 1999. Comparing palynological abundance and diversity: implications for biotic replacement during the Cretaceous angiosperm radiation. Paleobiology 25:305–340.Google Scholar
Lusk, C. H., Wright, I., and Reich, P. B. 2003. Photosynthetic differences contribute to competitive advantage of evergreen angiosperm trees over evergreen conifers in productive habitats. New Phytologist 160:329–336.CrossRefGoogle ScholarPubMed
Maddison, W. P., and Maddison, D. R. V. 2008. Mesquite: a modular system for evolutionary analysis. http://mesquiteproject.org Google Scholar
Martin, R. E. 1995. Cyclic and secular variation in microfossil biomineralization: clues to the biogeochemical evolution of Phanerozoic oceans. Global and Planetary Change 11:1–23.Google Scholar
McElwain, J. C., Willis, K. J., and Lupia, R. 2005. Cretaceous CO2 decline and the radiation and diversification of angiosperms. Pp. 133–165 in Ehleringer, J. R., Cerling, T. E., and Dearing, M. D., eds. A history of atmospheric CO2 and its effect on plants, animals, and ecosystems. Springer, New York.Google Scholar
McKown, A. D., Cochard, H., and Sack, L. 2010. Decoding leaf hydraulics with a spatially explicit model: principles of venation architecture and implication for its evolution. American Naturalist 175:447–460.Google Scholar
Merigliano, M. F. 2005. Cottonwood understory zonation and its relation to flood plain stratigraphy. Wetlands 25:356–374.Google Scholar
Moore, M. J., Bell, C. D., Soltis, P. S., and Soltis, D. E. 2007. Using plastid genome-scale data to resolve enigmatic relationships among basal angiosperms. Proceedings of the National Academy of Sciences USA 49:19363–19368.Google Scholar
Osborne, C. P., Beerling, D. J., Lomax, D. H., and Chaloner, W. G. 2004. Biophysical constraints on the origin of leaves inferred from the fossil record. Proceedings of the National Academy of Sciences USA 101:10360–10362.Google Scholar
Parlange, J. Y., and Waggoner, P. E. 1970. Stomatal dimensions and resistance to diffusion. Plant Physiology 46:337–348.Google Scholar
Puhakka, M., Kalliola, R., Rajasilta, M., and Salo, J. 1992. River types, site evolution, and successional vegetation patterns in Peruvian Amazonia. Journal of Biogeography 19:651–665.CrossRefGoogle Scholar
Retallack, G. J., and Dilcher, D. L. 1981. A coastal hypothesis for the dispersal and rise to dominance of flower plants. Pp. 27–77 in Niklas, K. J., ed. Paleobotany, paleoecology, and evolution. Praeger, New York.Google Scholar
Retallack, G. J., and Dilcher, D. L. 1986. Cretaceous angiosperm invasion of North America. Cretaceous Research 7:227–252.Google Scholar
Richardi-Branco, F., Branco, F. C., Garcia, R. J. F., Faria, R. S., Pereira, S. Y., Portugal, R., Pressenda, L. C., and Pereira, P. R. B. 2009. Plant accumulations along the Itanhaem River Basin, southern coast of Sao Paulo State, Brazil. Palaios 24:416–424.Google Scholar
Robertson, K. M., and Augspurger, C. K. 1999. Geomorphic processes and spatial patterns of primary forest succession on the Bogue Chitto River, United States of America. Journal of Ecology 87:1052–1063.Google Scholar
Robinson, J. M. 1994. Speculations on carbon dioxide starvation, Late Tertiary evolution of stomatal regulation and floristic modernization. Plant, Cell and Environment 17:1–10.Google Scholar
Rood, S. B., Braatne, J. H., and Hughes, F. M. R. 2003. Ecophysiology of riparian cottonwoods: stream flow dependency, water relations, and restoration. Tree Physiology 23:1113–1124.Google Scholar
Royer, D. L. 2010. Fossils constrain ancient climate sensitivity. Proceedings of the National Academy of Sciences USA 107:517–518.Google Scholar
Royer, D. L., Hickey, L. J., and Wing, S. 2003. Ecological conservatism in the ‘living fossil’ Ginkgo . Paleobiology 29:84–104.Google Scholar
Royer, D. L., Miller, I. M., Peppe, D. J., and Hickey, L. J. 2010. Leaf economic traits from fossils support a weedy habit for early angiosperms. American Journal of Botany 97:1–8.Google Scholar
Saarela, J. M., Rai, H. S., Doyle, J. A., Endress, P. K., Mathews, S., Marchant, A., Briggs, B., and Graham, S. W. 2007. A new branch emerges near the root of angiosperm phylogeny. Nature 446:312–315.Google Scholar
Sack, L., and Holbrook, N. M. 2006. Leaf hydraulics. Annual Review of Plant Biology 57:361–381.Google Scholar
Schönherr, J, and Bukovac, M. J. 1972. Dependence on surface tension, wettability, and stomatal morphology. Plant Physiology 49:813–819.Google Scholar
Sperry, J. S. 2003. Evolution of water transport and xylem structure. International Journal of Plant Sciences 164:S115–S127.Google Scholar
Sperry, J. S., Hacke, U. G., Feild, T. S., Sano, Y., and Sikkema, E. H. 2007. Hydraulic consequences of vessel evolution. International Journal of Plant Sciences 168:1127–1139.Google Scholar
Stebbins, G. L. 1974. Flowering plants: evolution above the species level. Harvard University Press, Cambridge.Google Scholar
Sun, G., and Dilcher, D. L. 2002. Early angiosperms from the Lower Cretaceous of Jixi, eastern Heilongjiang, China. Review of Palaeobotany and Palynology 121:91–112.Google Scholar
Taylor, D. W., and Hickey, L. J. 1996. Evidence for and implications of an herbaceous origin for angiosperms. Pp. 232–266 in Taylor, D. W. and Hickey, L. J., eds. Flowering plant origin, evolution, and phylogeny. Chapman and Hall, New York.CrossRefGoogle Scholar
Taylor, L. L., Leake, J. R., Quirk, J., Hardy, K., Banwart, S. A., and Beerling, D. J. 2009. Biological weathering and the long-term carbon cycle: integrating mycorrhizal evolution and function into the current paradigm. Geobiology 7:171–191.Google Scholar
Todzia, C. A., and Keating, R. C. 1991. Leaf architecture of the Chloranthaceae. Annals of the Missouri Botanical Garden 78:476–496.Google Scholar
Ufnar, D. F., Ludvigson, G. A., Gonzalez, L. A., and Gröcke, D. R. 2008. Precipitation rates and atmospheric heat transport during the Cenomanian greenhouse warming in North America: Estimates from a stable isotope mass-balance model. Palaeogeography, Palaeoclimatology, Palaeoecology 266:28–38.Google Scholar
Upchurch, G. R. 1984a. Cuticular anatomy of angiosperm leaves from the Lower Cretaceous Potomac Group. Zone I leaves. American Journal of Botany 71:192–2002.Google Scholar
Upchurch, G. R. 1984b. Cuticle evolution in Early Cretaceous angiosperms from the Potomac Group of Virginia and Maryland. Annals of the Missouri Botanical Garden 71:522–550.Google Scholar
Upchurch, G. R. 1995. Dispersed angiosperm cuticles: their history, preparation, and application to the rise of angiosperms in Cretaceous and Paleocene coals, south western interior of North America. International Journal of Coal Geology 28:161–227.Google Scholar
Upchurch, G. R., and Dilcher, D. L. 1990. Cenomanian angiosperm leaf megafossils, Dakota Formation, Rose Creek Locality, Jefferson County, Southeastern Nebraska. U.S. Geological Survey Bulletin 1915.Google Scholar
Upchurch, G. R., and Wolfe, J. A. 1987. Mid-Cretaceous to Early Tertiary vegetation and climate: evidence from fossil leaves and woods. Pp. 75–105 in Friis, E. M., Chaloner, W. G., and Crane, P. R., eds. The origins of angiosperms and their biological consequences. Cambridge University Press, Cambridge.Google Scholar
Van Gardingen, P. R., Jeffree, C. E., and Grace, J. 1989. Variation in stomatal aperture in leaves of Avena fatua L. observed by low temperature scanning electron microscopy. Plant, Cell, and Environment 12:887–897.CrossRefGoogle Scholar
Vermeij, G. J. 1999. Inequality and the directionality of history. American Naturalist 153:243–253.CrossRefGoogle ScholarPubMed
Volk, T. J. 1989. Rise of angiosperms as a factor in long-term climatic cooling. Geology 17:107–110.Google Scholar
Wang, H., and Dilcher, D. L. 2006. Early Cretaceous angiosperm leaves from the Dakota Formation, Braun Ranch locality, Kansas, United States of America. Palaeontographica, Abteilung B 273:101–137.Google Scholar
Wang, H., and Dilcher, D. L. 2009. Late Cretaceous angiosperm leaves from the Courtland Clay Pit, Minnesota. Palaeontographica, Abteilung B 281:143–177.CrossRefGoogle Scholar
White, T., Gonzalez, L., Ludvigson, G., and Poulson, C. 2001. Middle Cretaceous greenhouse hydrological cycle of North America. Geology 29:363–366.Google Scholar
Williams, J. H. 2008. Novelties of the flowering plant pollen tube underlie diversification of a key life history stage. Proceedings of the National Academy of Sciences USA 105:11259–11263.Google Scholar
Wing, S. L., and Boucher, L. D. 1998. Ecological aspects of the Cretaceous flowering plant radiation. Annual Review of Earth and Planetary Sciences 26:379–421.Google Scholar
Wullschleger, S. D. 1993. Biochemical limitations to carbon assimilation in C3—a retrospective analysis of the A/Ci curves from 109 species. Journal of Experimental Botany 44:907–920.Google Scholar
Wullschleger, S. D., Tschaplinski, T. J., and Norby, R. J. 2002. Plant water relations at elevated CO2 — implications for water-limited environments. Plant, Cell and Environment 25:319–331.Google Scholar
Supplementary material: PDF

Feild et al. supplementary material

Supplementary Material

Download Feild et al. supplementary material(PDF)
PDF 989.7 KB